Download PDF
CC BY 4.0 · TH Open 2025; 09: a25994925
DOI: 10.1055/a-2599-4925
Review Article

HSP47 at the Crossroads of Thrombosis and Collagen Dynamics: Unlocking Therapeutic Horizons and Debates

David M. Smadja 
1   Department of Hematology, Assistance Publique – Hôpitaux de Paris, Georges Pompidou European Hospital, Paris, France
2   Université Paris Cité, Institut National de la Santé et de la Recherche Médicale, Paris Cardiovascular Research Center, Paris, France
,
Alberto F. Chocron
3   Research Service, Miami Veteran Administration Medical Center, Miami, Florida, United States
4   Department of Medicine, BTT Medical Institute, Aventura, Florida, United States
,
M. Marc Abreu
4   Department of Medicine, BTT Medical Institute, Aventura, Florida, United States
5   Department of Engineering, BTT Medical Institute, Aventura, Florida, United States
› Author Affiliations
› Further Information
Also available at
  Permissions and Reprints

Abstract

Heat shock protein 47 (HSP47), a collagen-specific molecular chaperone encoded by the SERPINH1 gene, has emerged as a groundbreaking focus in thrombosis research. Recent findings published in “Science” have revolutionized our understanding of thrombosis, identifying HSP47 as a critical mediator in a new thrombosis target for treatment. This discovery not only unveils a novel pathway in thrombosis but also opens new avenues for therapeutic intervention. HSP47's significance extends beyond thrombosis, influencing pathological processes such as fibrosis and cancer. In fibrosis, its upregulation promotes collagen deposition, while its dysregulation in osteogenesis imperfecta (OI) Type X underscores the protein's indispensable role in collagen biosynthesis. The therapeutic challenge lies in balancing HSP47 inhibition to reduce fibrotic burden without impairing its essential physiological functions. In cancer, HSP47 plays dual roles. It supports tumor progression through collagen stabilization and metastasis facilitation while contributing to tissue repair under hyperthermia treatment combined with radiotherapy or chemotherapy. However, its overexpression can exacerbate tumor aggressiveness via mechanisms such as angiogenesis and epithelial–mesenchymal transition.

This review emphasizes the pivotal discovery of HSP47's thrombogenic role and its broader implications in disease biology. These findings mark a paradigm shift in thrombosis research and underscore the potential of HSP47 as a target in diverse pathological contexts, from platelet-driven diseases to fibrotic and oncological disorders.

Keywords

heat shock protein 47 - collagen - thrombosis - angiogenesis - cancer therapy - hyperthermia

Authors' Contributions

D.M.S. and M.M.A. supervised the work and wrote the paper. A.F.C. participated in writing and editing of the paper.




Publication History

Received: 05 February 2025

Accepted: 22 April 2025

Article published online:
05 June 2025

© 2025. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

Georg Thieme Verlag KG
Oswald-Hesse-Straße 50, 70469 Stuttgart, Germany

Bibliographical Record
David M. Smadja, Alberto F. Chocron, M. Marc Abreu. HSP47 at the Crossroads of Thrombosis and Collagen Dynamics: Unlocking Therapeutic Horizons and Debates. TH Open 2025; 09: a25994925.
DOI: 10.1055/a-2599-4925
 

  • References

  • 1 Ricard-Blum S. The collagen family. Cold Spring Harb Perspect Biol 2011; 3 (01) a004978
    Search in Google Scholar
  • 2 Shoulders MD, Raines RT. Collagen structure and stability. Annu Rev Biochem 2009; 78: 929-958
    Search in Google Scholar
  • 3 Fujii KK, Taga Y, Sakai T. et al. Lowering the culture temperature corrects collagen abnormalities caused by HSP47 gene knockout. Sci Rep 2019; 9 (01) 17433
    Search in Google Scholar
  • 4 Nagai N, Hosokawa M, Itohara S. et al. Embryonic lethality of molecular chaperone hsp47 knockout mice is associated with defects in collagen biosynthesis. J Cell Biol 2000; 150 (06) 1499-1506
    Search in Google Scholar
  • 5 Ito S, Nagata K. Roles of the endoplasmic reticulum-resident, collagen-specific molecular chaperone Hsp47 in vertebrate cells and human disease. J Biol Chem 2019; 294 (06) 2133-2141
    Search in Google Scholar
  • 6 Ito S, Nagata K. Biology of Hsp47 (Serpin H1), a collagen-specific molecular chaperone. Semin Cell Dev Biol 2017; 62: 142-151
    Search in Google Scholar
  • 7 Singh MK, Shin Y, Ju S. et al. Heat shock response and heat shock proteins: Current understanding and future opportunities in human diseases. Int J Mol Sci 2024; 25 (08) 4209
    Search in Google Scholar
  • 8 Niwa T, Kanamori T, Ueda T, Taguchi H. Global analysis of chaperone effects using a reconstituted cell-free translation system. Proc Natl Acad Sci U S A 2012; 109 (23) 8937-8942
    Search in Google Scholar
  • 9 Oecal S, Socher E, Uthoff M. et al. The pH-dependent client release from the collagen-specific chaperone HSP47 is triggered by a tandem histidine pair. J Biol Chem 2016; 291 (24) 12612-12626
    Search in Google Scholar
  • 10 Taguchi T, Razzaque MS. The collagen-specific molecular chaperone HSP47: is there a role in fibrosis?. Trends Mol Med 2007; 13 (02) 45-53
    Search in Google Scholar
  • 11 Bellaye P-S, Burgy O, Bonniaud P, Kolb M. HSP47: a potential target for fibrotic diseases and implications for therapy. Expert Opin Ther Targets 2021; 25 (01) 49-62
    Search in Google Scholar
  • 12 Kaiser WJ, Holbrook L-M, Tucker KL, Stanley RG, Gibbins JM. A functional proteomic method for the enrichment of peripheral membrane proteins reveals the collagen binding protein Hsp47 is exposed on the surface of activated human platelets. J Proteome Res 2009; 8 (06) 2903-2914
    Search in Google Scholar
  • 13 Sasikumar P, AlOuda KS, Kaiser WJ. et al. The chaperone protein HSP47: a platelet collagen binding protein that contributes to thrombosis and hemostasis. J Thromb Haemost 2018; 16 (05) 946-959
    Search in Google Scholar
  • 14 Thienel M, Müller-Reif JB, Zhang Z. et al. Immobility-associated thromboprotection is conserved across mammalian species from bear to human. Science 2023; 380 (6641): 178-187
    Search in Google Scholar
  • 15 Herbert A. Osteogenesis imperfecta type 10 and the cellular scaffolds underlying common immunological diseases. Genes Immun 2024; 25 (04) 265-276
    Search in Google Scholar
  • 16 Myllyharju J, Kivirikko KI. Collagens and collagen-related diseases. Ann Med 2001; 33 (01) 7-21
    Search in Google Scholar
  • 17 Kisseleva T, Brenner D. Molecular and cellular mechanisms of liver fibrosis and its regression. Nat Rev Gastroenterol Hepatol 2021; 18 (03) 151-166
    Search in Google Scholar
  • 18 Karsdal MA, Daniels SJ, Holm Nielsen S. et al. Collagen biology and non-invasive biomarkers of liver fibrosis. Liver Int 2020; 40 (04) 736-750
    Search in Google Scholar
  • 19 Staab-Weijnitz CA. Fighting the fiber: Targeting collagen in lung fibrosis. Am J Respir Cell Mol Biol 2022; 66 (04) 363-381
    Search in Google Scholar
  • 20 Bülow RD, Boor P. Extracellular matrix in kidney fibrosis: More than just a scaffold. J Histochem Cytochem 2019; 67 (09) 643-661
    Search in Google Scholar
  • 21 Eddy AA. Overview of the cellular and molecular basis of kidney fibrosis. Kidney Int Suppl (2011) 2014; 4 (01) 2-8
    Search in Google Scholar
  • 22 Zhang X, Zhang X, Huang W, Ge X. The role of heat shock proteins in the regulation of fibrotic diseases. Biomed Pharmacother 2021; 135: 111067
    Search in Google Scholar
  • 23 Miyamura T, Sakamoto N, Kakugawa T. et al. Small molecule inhibitor of HSP47 prevents pro-fibrotic mechanisms of fibroblasts in vitro. Biochem Biophys Res Commun 2020; 530 (03) 561-565
    Search in Google Scholar
  • 24 Bellaye P-S, Burgy O, Causse S, Garrido C, Bonniaud P. Heat shock proteins in fibrosis and wound healing: good or evil?. Pharmacol Ther 2014; 143 (02) 119-132
    Search in Google Scholar
  • 25 Ishii H, Mukae H, Kakugawa T. et al. Increased expression of collagen-binding heat shock protein 47 in murine bleomycin-induced pneumopathy. Am J Physiol Lung Cell Mol Physiol 2003; 285 (04) L957-L963
    Search in Google Scholar
  • 26 Kakugawa T, Mukae H, Hishikawa Y. et al. Localization of HSP47 mRNA in murine bleomycin-induced pulmonary fibrosis. Virchows Arch 2010; 456 (03) 309-315
    Search in Google Scholar
  • 27 Ham SY, Pyo MJ, Kang M. et al. HSP47 increases the expression of type I collagen in fibroblasts through IRE1α activation, XBP1 splicing, and nuclear translocation of β-catenin. Cells 2024; 13 (06) 527
    Search in Google Scholar
  • 28 Nakayama S, Mukae H, Sakamoto N. et al. Pirfenidone inhibits the expression of HSP47 in TGF-beta1-stimulated human lung fibroblasts. Life Sci 2008; 82 (3-4): 210-217
    Search in Google Scholar
  • 29 Hisatomi K, Mukae H, Sakamoto N. et al. Pirfenidone inhibits TGF-β1-induced over-expression of collagen type I and heat shock protein 47 in A549 cells. BMC Pulm Med 2012; 12: 24
    Search in Google Scholar
  • 30 Kakugawa T, Mukae H, Hayashi T. et al. Expression of HSP47 in usual interstitial pneumonia and nonspecific interstitial pneumonia. Respir Res 2005; 6 (01) 57
    Search in Google Scholar
  • 31 Kim DJ, Park SH, Sheen MR. et al. Comparison of experimental lung injury from acute renal failure with injury due to sepsis. Respiration 2006; 73 (06) 815-824
    Search in Google Scholar
  • 32 Razzaque MS, Nazneen A, Taguchi T. Immunolocalization of collagen and collagen-binding heat shock protein 47 in fibrotic lung diseases. Mod Pathol 1998; 11 (12) 1183-1188
    Search in Google Scholar
  • 33 Iwashita T, Kadota J, Naito S. et al. Involvement of collagen-binding heat shock protein 47 and procollagen type I synthesis in idiopathic pulmonary fibrosis: contribution of type II pneumocytes to fibrosis. Hum Pathol 2000; 31 (12) 1498-1505
    Search in Google Scholar
  • 34 Sakamoto N, Okuno D, Tokito T. et al. HSP47: A therapeutic target in pulmonary fibrosis. Biomedicines 2023; 11 (09) 2387
    Search in Google Scholar
  • 35 Yokota S, Kubota H, Matsuoka Y. et al. Prevalence of HSP47 antigen and autoantibodies to HSP47 in the sera of patients with mixed connective tissue disease. Biochem Biophys Res Commun 2003; 303 (02) 413-418
    Search in Google Scholar
  • 36 Hilberg F, Roth GJ, Krssak M. et al. BIBF 1120: triple angiokinase inhibitor with sustained receptor blockade and good antitumor efficacy. Cancer Res 2008; 68 (12) 4774-4782
    Search in Google Scholar
  • 37 Hostettler KE, Zhong J, Papakonstantinou E. et al. Anti-fibrotic effects of nintedanib in lung fibroblasts derived from patients with idiopathic pulmonary fibrosis. Respir Res 2014; 15 (01) 157
    Search in Google Scholar
  • 38 Wollin L, Wex E, Pautsch A. et al. Mode of action of nintedanib in the treatment of idiopathic pulmonary fibrosis. Eur Respir J 2015; 45 (05) 1434-1445
    Search in Google Scholar
  • 39 Wollin L, Distler JHW, Redente EF. et al. Potential of nintedanib in treatment of progressive fibrosing interstitial lung diseases. Eur Respir J 2019; 54 (03) 1900161
    Search in Google Scholar
  • 40 Wollin L, Maillet I, Quesniaux V, Holweg A, Ryffel B. Antifibrotic and anti-inflammatory activity of the tyrosine kinase inhibitor nintedanib in experimental models of lung fibrosis. J Pharmacol Exp Ther 2014; 349 (02) 209-220
    Search in Google Scholar
  • 41 Knüppel L, Ishikawa Y, Aichler M. et al. A novel antifibrotic mechanism of nintedanib and pirfenidone. Inhibition of collagen fibril assembly. Am J Respir Cell Mol Biol 2017; 57 (01) 77-90
    Search in Google Scholar
  • 42 Lehmann M, Buhl L, Alsafadi HN. et al. Differential effects of Nintedanib and Pirfenidone on lung alveolar epithelial cell function in ex vivo murine and human lung tissue cultures of pulmonary fibrosis. Respir Res 2018; 19 (01) 175
    Search in Google Scholar
  • 43 Wu W, Qiu L, Wu J, Liu X, Zhang G. Efficacy and safety of pirfenidone in the treatment of idiopathic pulmonary fibrosis patients: a systematic review and meta-analysis of randomised controlled trials. BMJ Open 2021; 11 (12) e050004
    Search in Google Scholar
  • 44 Kalayarasan S, Sriram N, Sudhandiran G. Diallyl sulfide attenuates bleomycin-induced pulmonary fibrosis: critical role of iNOS, NF-kappaB, TNF-alpha and IL-1beta. Life Sci 2008; 82 (23-24): 1142-1153
    Search in Google Scholar
  • 45 Chen L, Wang T, Wang X. et al. Blockade of advanced glycation end product formation attenuates bleomycin-induced pulmonary fibrosis in rats. Respir Res 2009; 10 (01) 55
    Search in Google Scholar
  • 46 Liu J, Jin Z, Wang X, Jakoš T, Zhu J, Yuan Y. RAGE pathways play an important role in regulation of organ fibrosis. Life Sci 2023; 323: 121713
    Search in Google Scholar
  • 47 Goulet S, Bihl MP, Gambazzi F, Tamm M, Roth M. Opposite effect of corticosteroids and long-acting beta(2)-agonists on serum- and TGF-beta(1)-induced extracellular matrix deposition by primary human lung fibroblasts. J Cell Physiol 2007; 210 (01) 167-176
    Search in Google Scholar
  • 48 Vergoten G, Bailly C. Insights into the mechanism of action of the degraded limonoid prieurianin. Int J Mol Sci 2024; 25 (07) 3597
    Search in Google Scholar
  • 49 Satoh M, Hirayoshi K, Yokota S, Hosokawa N, Nagata K. Intracellular interaction of collagen-specific stress protein HSP47 with newly synthesized procollagen. J Cell Biol 1996; 133 (02) 469-483
    Search in Google Scholar
  • 50 Ko MK, Kay EP. Hsp47-dependent and -independent intracellular trafficking of type I collagen in corneal endothelial cells. Mol Vis 1999; 5: 17
    Search in Google Scholar
  • 51 Liu Y, Liu J, Quimbo A. et al. Anti-HSP47 siRNA lipid nanoparticle ND-L02-s0201 reverses interstitial pulmonary fibrosis in preclinical rat models. ERJ Open Res 2021; 7 (02) 00733-02020
    Search in Google Scholar
  • 52 Okuno D, Sakamoto N, Tagod MSO. et al. Screening of inhibitors targeting heat shock protein 47 involved in the development of idiopathic pulmonary fibrosis. ChemMedChem 2021; 16 (16) 2515-2523
    Search in Google Scholar
  • 53 Wu S, Liang C, Xie X. et al. Hsp47 inhibitor Col003 attenuates collagen-induced platelet activation and cerebral ischemic-reperfusion injury in rats. Front Pharmacol 2022; 12: 792263
    Search in Google Scholar
  • 54 Chen J-J, Jin P-S, Zhao S. et al. Effect of heat shock protein 47 on collagen synthesis of keloid in vivo. ANZ J Surg 2011; 81 (06) 425-430
    Search in Google Scholar
  • 55 Hagiwara S, Iwasaka H, Matsumoto S, Noguchi T. An antisense oligonucleotide to HSP47 inhibits paraquat-induced pulmonary fibrosis in rats. Toxicology 2007; 236 (03) 199-207
    Search in Google Scholar
  • 56 Hagiwara S, Iwasaka H, Matsumoto S, Noguchi T. Antisense oligonucleotide inhibition of heat shock protein (HSP) 47 improves bleomycin-induced pulmonary fibrosis in rats. Respir Res 2007; 8 (01) 37
    Search in Google Scholar
  • 57 Huang J-Q, Tao R, Li L. et al. Involvement of heat shock protein 47 in Schistosoma japonicum-induced hepatic fibrosis in mice. Int J Parasitol 2014; 44 (01) 23-35
    Search in Google Scholar
  • 58 Morry J, Ngamcherdtrakul W, Gu S. et al. Dermal delivery of HSP47 siRNA with NOX4-modulating mesoporous silica-based nanoparticles for treating fibrosis. Biomaterials 2015; 66: 41-52
    Search in Google Scholar
  • 59 Xia Z, Abe K, Furusu A. et al. Suppression of renal tubulointerstitial fibrosis by small interfering RNA targeting heat shock protein 47. Am J Nephrol 2008; 28 (01) 34-46
    Search in Google Scholar
  • 60 Obata Y, Nishino T, Kushibiki T. et al. HSP47 siRNA conjugated with cationized gelatin microspheres suppresses peritoneal fibrosis in mice. Acta Biomater 2012; 8 (07) 2688-2696
    Search in Google Scholar
  • 61 Sato Y, Murase K, Kato J. et al. Resolution of liver cirrhosis using vitamin A-coupled liposomes to deliver siRNA against a collagen-specific chaperone. Nat Biotechnol 2008; 26 (04) 431-442
    Search in Google Scholar
  • 62 Ishiwatari H, Sato Y, Murase K. et al. Treatment of pancreatic fibrosis with siRNA against a collagen-specific chaperone in vitamin A-coupled liposomes. Gut 2013; 62 (09) 1328-1339
    Search in Google Scholar
  • 63 Otsuka M, Shiratori M, Chiba H. et al. Treatment of pulmonary fibrosis with siRNA against a collagen-specific chaperone HSP47 in vitamin A-coupled liposomes. Exp Lung Res 2017; 43 (6-7): 271-282
    Search in Google Scholar
  • 64 Ohigashi H, Hashimoto D, Hayase E. et al. Ocular instillation of vitamin A-coupled liposomes containing HSP47 siRNA ameliorates dry eye syndrome in chronic GVHD. Blood Adv 2019; 3 (07) 1003-1010
    Search in Google Scholar
  • 65 Yamakawa T, Ohigashi H, Hashimoto D. et al. Vitamin A-coupled liposomes containing siRNA against HSP47 ameliorate skin fibrosis in chronic graft-versus-host disease. Blood 2018; 131 (13) 1476-1485
    Search in Google Scholar
  • 66 Zhu J, Xiong G, Fu H, Evers BM, Zhou BP, Xu R. Chaperone Hsp47 drives malignant growth and invasion by modulating an ECM gene network. Cancer Res 2015; 75 (08) 1580-1591
    Search in Google Scholar
  • 67 Mori K, Toiyama Y, Okugawa Y. et al. Preoperative heat shock protein 47 levels identify colorectal cancer patients with lymph node metastasis and poor prognosis. Oncol Lett 2020; 20 (06) 333
    Search in Google Scholar
  • 68 Mori K, Toiyama Y, Otake K. et al. Proteomics analysis of differential protein expression identifies heat shock protein 47 as a predictive marker for lymph node metastasis in patients with colorectal cancer. Int J Cancer 2017; 140 (06) 1425-1435
    Search in Google Scholar
  • 69 Huang X, Gollin SM, Raja S, Godfrey TE. High-resolution mapping of the 11q13 amplicon and identification of a gene, TAOS1, that is amplified and overexpressed in oral cancer cells. Proc Natl Acad Sci U S A 2002; 99 (17) 11369-11374
    Search in Google Scholar
  • 70 Shi R, Yu R, Lian F. et al. Targeting HSP47 for cancer treatment. Anticancer Drugs 2024; 35 (07) 623-637
    Search in Google Scholar
  • 71 Xiong G, Chen J, Zhang G. et al. Hsp47 promotes cancer metastasis by enhancing collagen-dependent cancer cell-platelet interaction. Proc Natl Acad Sci U S A 2020; 117 (07) 3748-3758
    Search in Google Scholar
  • 72 Tian S, Peng P, Li J. et al. SERPINH1 regulates EMT and gastric cancer metastasis via the Wnt/β-catenin signaling pathway. Aging (Albany NY) 2020; 12 (04) 3574-3593
    Search in Google Scholar
  • 73 Chen J, Wang S, Zhang Z, Richards CI, Xu R. Heat shock protein 47 (HSP47) binds to discoidin domain-containing receptor 2 (DDR2) and regulates its protein stability. J Biol Chem 2019; 294 (45) 16846-16854
    Search in Google Scholar
  • 74 Yoneda A, Minomi K, Tamura Y. HSP47 promotes metastasis of breast cancer by interacting with myosin IIA via the unfolded protein response transducer IRE1α. Oncogene 2020; 39 (23) 4519-4537
    Search in Google Scholar
  • 75 Wu ZB, Cai L, Lin SJ. et al. Heat shock protein 47 promotes glioma angiogenesis. Brain Pathol 2016; 26 (01) 31-42
    Search in Google Scholar
  • 76 Ma W, Ou T, Cui X. et al. HSP47 contributes to angiogenesis by induction of CCL2 in bladder cancer. Cell Signal 2021; 85: 110044
    Search in Google Scholar
  • 77 Recchia FM, Xu L. Differential expression of the collagen-binding protein Hsp47 in experimental retinal neovascularization. Invest Ophthalmol Vis Sci 2005; 46: 3162
    Search in Google Scholar
  • 78 Wendelboe A, Weitz JI. Global health burden of venous thromboembolism. Arterioscler Thromb Vasc Biol 2024; 44 (05) 1007-1011
    Search in Google Scholar
  • 79 Khan F, Tritschler T, Kahn SR, Rodger MA. Venous thromboembolism. Lancet 2021; 398 (10294): 64-77
    Search in Google Scholar
  • 80 AlOuda SK, Sasikumar P, AlThunayan T. et al. Role of heat shock protein 47 in platelet glycoprotein VI dimerization and signaling. Res Pract Thromb Haemost 2023; 7 (06) 102177
    Search in Google Scholar
  • 81 Crescente M, Pluthero FG, Li L. et al. Intracellular trafficking, localization, and mobilization of platelet-borne Thiol isomerases. Arterioscler Thromb Vasc Biol 2016; 36 (06) 1164-1173
    Search in Google Scholar
  • 82 Liu D, Razzaque MS, Cheng M, Taguchi T. The renal expression of heat shock protein 47 and collagens in acute and chronic experimental diabetes in rats. Histochem J 2001; 33 (11-12): 621-628
    Search in Google Scholar
  • 83 Manderstedt E, Lind-Halldén C, Halldén C. et al.; Regeneron Genetics Center. SERPINH1 variants and thrombotic risk among middle-aged and older adults: a population-based cohort study. J Thromb Haemost 2024; 22 (03) 869-873
    Search in Google Scholar
  • 84 Cai H, Sasikumar P, Little G. et al. Identification of HSP47 binding site on native collagen and its implications for the development of HSP47 inhibitors. Biomolecules 2021; 11 (07) 983
    Search in Google Scholar
  • 85 Charles S, Fatrara T, Bouriche T. et al. Tissue factor-bearing extracellular vesicles, procoagulant phospholipids and D-dimer as potential biomarkers for venous thromboembolism in patients with newly diagnosed multiple myeloma: A comprehensive analysis. Thromb Res 2025; 247: 109256
    Search in Google Scholar
  • 86 Lucotti S, Ogitani Y, Kenific CM. et al. Extracellular vesicles from the lung pro-thrombotic niche drive cancer-associated thrombosis and metastasis via integrin beta 2. Cell 2025; 188 (06) 1642-1661.e24
    Search in Google Scholar
  • 87 Shibata C, Otsuka M, Ishigaki K, Seimiya T, Kishikawa T, Fujishiro M. CA19-9-positive extracellular vesicle is a risk factor for cancer-associated thrombosis in pancreatic cancer. Gastro Hep Adv 2024; 3 (04) 551-561
    Search in Google Scholar
  • 88 Osorio LA, Lozano M, Soto P. et al. Levels of small extracellular vesicles containing hERG-1 and Hsp47 as potential biomarkers for cardiovascular diseases. Int J Mol Sci 2024; 25 (09) 4913
    Search in Google Scholar
  • 89 Kajikawa Y, Morihara T, Sakamoto H. et al. Platelet-rich plasma enhances the initial mobilization of circulation-derived cells for tendon healing. J Cell Physiol 2008; 215 (03) 837-845
    Search in Google Scholar
  • 90 Wu C-L, Lee S-S, Tsai C-H, Lu KH, Zhao JH, Chang YC. Platelet-rich fibrin increases cell attachment, proliferation and collagen-related protein expression of human osteoblasts. Aust Dent J 2012; 57 (02) 207-212
    Search in Google Scholar
  • 91 Junkiert-Czarnecka A, Pilarska-Deltow M, Bąk A, Heise M, Haus O. The role of gene encoding collagen secretion protein (SERPINH1) in the pathogenesis of a hypermobile type of Ehlers-Danlos syndrome. Postepy Dermatol Alergol 2023; 40 (01) 102-106
    Search in Google Scholar
  • 92 Smadja DM. Hyperthermia for targeting cancer and cancer stem cells: Insights from novel cellular and clinical approaches. Stem Cell Rev Rep 2024; 20 (06) 1532-1539
    Search in Google Scholar
  • 93 Mallory M, Gogineni E, Jones GC, Greer L, Simone II CB. Therapeutic hyperthermia: The old, the new, and the upcoming. Crit Rev Oncol Hematol 2016; 97: 56-64
    Search in Google Scholar
  • 94 Smadja DM, Abreu MM. Hyperthermia and targeting heat shock proteins: innovative approaches for neurodegenerative disorders and Long COVID. Front Neurosci 2025; 19: 1475376
    Search in Google Scholar
  • 95 Abreu MM, Chocron AF, Smadja DM. From cold to hot: mechanisms of hyperthermia in modulating tumor immunology for enhanced immunotherapy. Front Immunol 2025; 16: 1487296
    Search in Google Scholar
  • 96 Lukácsi S, Munkácsy G, Győrffy B. Harnessing hyperthermia: Molecular, cellular, and immunological insights for enhanced anticancer therapies. Integr Cancer Ther 2024; 23: 15 347354241242094
    Search in Google Scholar
  • 97 Sharma HS, Hoopes PJ. Hyperthermia induced pathophysiology of the central nervous system. Int J Hyperthermia 2003; 19 (03) 325-354
    Search in Google Scholar
  • 98 Beemelmanns A, Zanuzzo FS, Xue X, Sandrelli RM, Rise ML, Gamperl AK. The transcriptomic responses of Atlantic salmon (Salmo salar) to high temperature stress alone, and in combination with moderate hypoxia. BMC Genomics 2021; 22 (01) 261
    Search in Google Scholar
  • 99 Akbarzadeh A, Günther OP, Houde AL. et al. Developing specific molecular biomarkers for thermal stress in salmonids. BMC Genomics 2018; 19 (01) 749
    Search in Google Scholar
  • 100 Nagata K, Saga S, Yamada KM. A major collagen-binding protein of chick embryo fibroblasts is a novel heat shock protein. J Cell Biol 1986; 103 (01) 223-229
    Search in Google Scholar
  • 101 Verrico AK, Haylett AK, Moore JV. In vivo expression of the collagen-related heat shock protein HSP47, following hyperthermia or photodynamic therapy. Lasers Med Sci 2001; 16 (03) 192-198
    Search in Google Scholar
  • 102 Abdelnasir A, Sun JR, Cheng YF. et al. Evaluation of Hsp47 expression in heat-stressed rat myocardial cells in vitro and in vivo. Genet Mol Res 2014; 13 (04) 10787-10802
    Search in Google Scholar
  • 103 Dams SD, De Liefde-van Beest M, Nuijs AM. et al. Pulsed heat shocks enhance procollagen type I and procollagen type III expression in human dermal fibroblasts. Skin Res Technol 2010; 16: 354-364 . Accessed October 1, 2024 at: https://onlinelibrary.wiley.com/doi/10.1111/j.1600-0846.2010.00441.x
    Search in Google Scholar
  • 104 Haylett AK, Higley K, Chiu M, Shackley DC, Moore JV. Collagen secretion after photodynamic therapy versus scar-inducing anti-cancer modalities: an in vitro study. Photochem Photobiol Sci 2002; 1 (09) 673-677
    Search in Google Scholar
  • 105 Shackley DC, Haylett A, Whitehurst C. et al. Comparison of the cellular molecular stress responses after treatments used in bladder cancer. BJU Int 2002; 90 (09) 924-932
    Search in Google Scholar
  • 106 Verrico AK, Moore JV. Expression of the collagen-related heat shock protein HSP47 in fibroblasts treated with hyperthermia or photodynamic therapy. Br J Cancer 1997; 76 (06) 719-724
    Search in Google Scholar
  • 107 Miyaishi O, Ito Y, Kozaki K. et al. Age-related attenuation of HSP47 heat response in fibroblasts. Mech Ageing Dev 1995; 77 (03) 213-226
    Search in Google Scholar
  • 108 Tong M, Zhang S, Ma P. et al. Efficacy analysis of intermittent pneumatic compression combined with hyperthermia at different temperatures for prevention of deep vein thrombosis after simulated orthopaedic surgery in male rabbits. Am J Transl Res 2024; 16 (10) 5337-5346
    Search in Google Scholar
  • 109 Khan ES, Däinghaus T. HSP47 in human diseases: Navigating pathophysiology, diagnosis and therapy. Clin Transl Med 2024; 14 (08) e1755
    Search in Google Scholar
  • 110 Morito D, Nagata K. ER stress proteins in autoimmune and inflammatory diseases. Front Immunol 2012; 3: 48
    Search in Google Scholar
  • 111 Fujimoto M, Hamaguchi Y, Yazawa N, Komura K, Takehara K, Sato S. Autoantibodies to a collagen-specific molecular chaperone, heat-shock protein 47, in systemic sclerosis. Clin Exp Immunol 2004; 138 (03) 534-539
    Search in Google Scholar
  • 112 Kakugawa T, Yokota S, Mukae H. et al. High serum concentrations of autoantibodies to HSP47 in nonspecific interstitial pneumonia compared with idiopathic pulmonary fibrosis. BMC Pulm Med 2008; 8: 23
    Search in Google Scholar
  • 113 Izquierdo E, Cañete JD, Celis R. et al. Synovial fibroblast hyperplasia in rheumatoid arthritis: clinicopathologic correlations and partial reversal by anti-tumor necrosis factor therapy. Arthritis Rheum 2011; 63 (09) 2575-2583
    Search in Google Scholar
  • 114 Kalayarasan S, Sriram N, Sudhandiran G. Life Sci 2008; 82 (23-24): 1142-1153
    Search in Google Scholar
  • 115 Liu Y, Liu J, Quimbo A. et al Anti-HSP47 siRNA lipid nanoparticle ND-L02-s0201 reverses interstitial pulmonary fibrosis in preclinical rat models. ERJ Open Res 2021; 7 (02) 0733-2020
    Search in Google Scholar