Download PDF
Semin Reprod Med 2007; 25(4): 287-299
DOI: 10.1055/s-2007-980222
Copyright © 2007 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA.

Engineering the Follicle Microenvironment

Erin R. West1 , Lonnie D. Shea1 , 2 , 3 , Teresa K. Woodruff2 , 3 , 4
  • 1Department of Chemical and Biological Engineering, Northwestern University, Evanston, Illinois
  • 2Center for Reproductive Research, Northwestern University, Evanston, Illinois
  • 3The Robert H. Lurie Comprehensive Cancer Center of Northwestern University, Chicago, Illinois
  • 4Department of Obstetrics and Gynecology, The Feinberg School of Medicine, Northwestern University, Chicago, Illinois
Further Information

Publication History

Publication Date:
26 June 2007 (online)

    Permissions and Reprints

ABSTRACT

In vitro ovarian follicle culture provides a tool to investigate folliculogenesis, and may one day provide women with fertility-preservation options. The application of tissue engineering principles to ovarian follicle maturation may enable the creation of controllable microenvironments that will coordinate the growth of the multiple cellular compartments within the follicle. Three-dimensional culture systems can preserve follicle architecture, thereby maintaining critical cell-cell and cell-matrix signaling lost in traditional two-dimensional attached follicle culture systems. Maintaining the follicular structure while manipulating the biochemical and mechanical environment will enable the development of controllable systems to investigate the fundamental biological principles underlying follicle maturation. This review describes recent advances in ovarian follicle culture, and highlights the tissue engineering principles that may be applied to follicle culture, with the ultimate objective of germline preservation for females facing premature infertility.

KEYWORDS

Follicle - ovary - biomaterials - alginate - tissue engineering

REFERENCES

  • 1 Nayudu P L, Fehrenbach A, Kiesel P et al.. Progress toward understanding follicle development in vitro: appearances are not deceiving.  Arch Med Res. 2001;  32 587-594
    CrossrefPubMedGoogle Scholar
  • 2 Senbon S, Hirao Y, Miyano T. Interactions between the oocyte and surrounding somatic cells in follicular development: lessons from in vitro culture.  J Reprod Dev. 2003;  49 259-269
    CrossrefPubMedGoogle Scholar
  • 3 Abir R, Nitke S, Ben-Haroush A et al.. In vitro maturation of human primordial ovarian follicles: clinical significance, progress in mammals, and methods for growth evaluation.  Histol Histopathol. 2006;  21 887-898
    PubMedGoogle Scholar
  • 4 Thomas F H, Walters K A, Telfer E E. How to make a good oocyte: an update on in-vitro models to study follicle regulation.  Hum Reprod Update. 2003;  9 541-555
    CrossrefPubMedGoogle Scholar
  • 5 Demeestere I, Centner J, Gervy C et al.. Impact of various endocrine and paracrine factors on in vitro culture of preantral follicles in rodents.  Reproduction. 2005;  130 147-156
    CrossrefPubMedGoogle Scholar
  • 6 Ksiazkiewicz L K. Recent achievements in in vitro culture and preservation of ovarian follicles in mammals.  Reprod Biol. 2006;  6 3-16
    PubMedGoogle Scholar
  • 7 Kreeger P K, Deck J W, Woodruff T K et al.. The in vitro regulation of ovarian follicle development using alginate-extracellular matrix gels.  Biomaterials. 2006;  27 714-723
    CrossrefPubMedGoogle Scholar
  • 8 Xu M, Kreeger P K, Shea L D et al.. Tissue engineered follicles produce live, fertile offspring.  Tissue Eng. 2006;  , In press
    PubMedGoogle Scholar
  • 9 Xu M, West E, Shea L D et al.. Identification of a stage-specific permissive in vitro culture environment for follicle growth and oocyte development.  Biol Reprod. 2006;  75 916-923
    CrossrefPubMedGoogle Scholar
  • 10 Eppig J J. Mouse oocyte development in vitro with various culture systems.  Dev Biol. 1977;  60 371-388
    CrossrefPubMedGoogle Scholar
  • 11 McGee E A, Hsueh A J. Initial and cyclic recruitment of ovarian follicles.  Endocr Rev. 2000;  21 200-214
    CrossrefPubMedGoogle Scholar
  • 12 Irving-Rodgers H F, Rodgers R J. Extracellular matrix of the developing ovarian follicle.  Semin Reprod Med. 2006;  24 195-203
    Article in Thieme ConnectPubMedGoogle Scholar
  • 13 Rodgers R J, Irving-Rodgers H F, Russell D L. Extracellular matrix of the developing ovarian follicle.  Reproduction. 2003;  126 415-424
    CrossrefPubMedGoogle Scholar
  • 14 Irving-Rodgers H F, Rodgers R J. Extracellular matrix in ovarian follicular development and disease.  Cell Tissue Res. 2005;  322 89-98
    PubMedGoogle Scholar
  • 15 Rodgers R J, Irving-Rodgers H F, van Wezel I L. Extracellular matrix in ovarian follicles.  Mol Cell Endocrinol. 2000;  163 73-79
    CrossrefPubMedGoogle Scholar
  • 16 Berkholtz C B, Shea L D, Woodruff T K. Extracellular matrix functions in follicle maturation.  Semin Reprod Med. 2006;  24 262-269
    Article in Thieme ConnectPubMedGoogle Scholar
  • 17 Albertini D F, Combelles C M, Benecchi E et al.. Cellular basis for paracrine regulation of ovarian follicle development.  Reproduction. 2001;  121 647-653
    CrossrefPubMedGoogle Scholar
  • 18 Albertini D F, Fawcett D W, Olds P J. Morphological variations in gap junctions of ovarian granulosa cells.  Tissue Cell. 1975;  7 389-405
    CrossrefPubMedGoogle Scholar
  • 19 Anderson E, Albertini D F. Gap junctions between the oocyte and companion follicle cells in the mammalian ovary.  J Cell Biol. 1976;  71 680-686
    CrossrefPubMedGoogle Scholar
  • 20 Edry I, Sela-Abramovich S, Dekel N. Meiotic arrest of oocytes depends on cell-to-cell communication in the ovarian follicle.  Mol Cell Endocrinol. 2006;  252 102-106
    CrossrefPubMedGoogle Scholar
  • 21 Cecconi S, Ciccarelli C, Barberi M et al.. Granulosa cell-oocyte interactions.  Eur J Obstet Gynecol Reprod Biol. 2004;  115(suppl 1) S19-S22
    CrossrefPubMedGoogle Scholar
  • 22 Kidder G M, Mhawi A A. Gap junctions and ovarian folliculogenesis.  Reproduction. 2002;  123 613-620
    CrossrefPubMedGoogle Scholar
  • 23 Plancha C E, Sanfins A, Rodrigues P et al.. Cell polarity during folliculogenesis and oogenesis.  Reprod Biomed Online. 2005;  10 478-484
    PubMedGoogle Scholar
  • 24 Bornslaeger E A, Schultz R M. Regulation of mouse oocyte maturation: effect of elevating cumulus cell cAMP on oocyte cAMP levels.  Biol Reprod. 1985;  33 698-704
    CrossrefPubMedGoogle Scholar
  • 25 Dekel N, Lawrence T S, Gilula N B et al.. Modulation of cell-to-cell communication in the cumulus-oocyte complex and the regulation of oocyte maturation by LH.  Dev Biol. 1981;  86 356-362
    CrossrefPubMedGoogle Scholar
  • 26 Gilula N B, Epstein M L, Beers W H. Cell-to-cell communication and ovulation. A study of the cumulus-oocyte complex.  J Cell Biol. 1978;  78 58-75
    CrossrefPubMedGoogle Scholar
  • 27 Martinovitch P N. The development in vitro of the mammalian gonad. Ovary and ovogenesis.  Proc R Soc Lond B Biol Sci. 1938;  125 232-249
    PubMedGoogle Scholar
  • 28 O'Brien M J, Pendola J K, Eppig J J. A revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence.  Biol Reprod. 2003;  68 1682-1686
    PubMedGoogle Scholar
  • 29 Eppig J J, O'Brien M J. Development in vitro of mouse oocytes from primordial follicles.  Biol Reprod. 1996;  54 197-207
    CrossrefPubMedGoogle Scholar
  • 30 Cortvrindt R, Smitz J, Van Steirteghem A C. In-vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepuberal mice in a simplified culture system.  Hum Reprod. 1996;  11 2656-2666
    PubMedGoogle Scholar
  • 31 Cecconi S, Gualtieri G, Di Bartolomeo A et al.. Evaluation of the effects of extremely low frequency electromagnetic fields on mammalian follicle development.  Hum Reprod. 2000;  15 2319-2325
    CrossrefPubMedGoogle Scholar
  • 32 Eppig J J, Schroeder A C. Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro.  Biol Reprod. 1989;  41 268-276
    CrossrefPubMedGoogle Scholar
  • 33 Daniel S A, Armstrong D T, Gore-Langton R E. Growth and development of rat oocytes in vitro.  Gamete Res. 1989;  24 109-121
    CrossrefPubMedGoogle Scholar
  • 34 Eppig J J, Downs S M. The effect of hypoxanthine on mouse oocyte growth and development in vitro: maintenance of meiotic arrest and gonadotropin-induced oocyte maturation.  Dev Biol. 1987;  119 313-321
    CrossrefPubMedGoogle Scholar
  • 35 Schroeder A C, Schultz R M, Kopf G S et al.. Fetuin inhibits zona pellucida hardening and conversion of ZP2 to ZP2f during spontaneous mouse oocyte maturation in vitro in the absence of serum.  Biol Reprod. 1990;  43 891-897
    CrossrefPubMedGoogle Scholar
  • 36 Eppig J J, Hosoe M, O'Brien M J et al.. Conditions that affect acquisition of developmental competence by mouse oocytes in vitro: FSH, insulin, glucose and ascorbic acid.  Mol Cell Endocrinol. 2000;  163 109-116
    CrossrefPubMedGoogle Scholar
  • 37 Gore-Langton R E, Daniel S A. Follicle-stimulating hormone and estradiol regulate antrum-like reorganization of granulosa cells in rat preantral follicle cultures.  Biol Reprod. 1990;  43 65-72
    PubMedGoogle Scholar
  • 38 Li R, Phillips D M, Mather J P. Activin promotes ovarian follicle development in vitro.  Endocrinology. 1995;  136 849-856
    CrossrefPubMedGoogle Scholar
  • 39 Cain L, Chatterjee S, Collins T J. In vitro folliculogenesis of rat preantral follicles.  Endocrinology. 1995;  136 3369-3377
    CrossrefPubMedGoogle Scholar
  • 40 Eppig J J, Telfer E E. Isolation and culture of oocytes.  Methods Enzymol. 1993;  225 77-84
    PubMedGoogle Scholar
  • 41 Gutierrez C G, Ralph J H, Telfer E E et al.. Growth and antrum formation of bovine preantral follicles in long-term culture in vitro.  Biol Reprod. 2000;  62 1322-1328
    CrossrefPubMedGoogle Scholar
  • 42 Tambe S S, Nandedkar T D. Steroidogenesis in sheep ovarian antral follicles in culture: time course study and supplementation with a precursor.  Steroids. 1993;  58 379-383
    CrossrefPubMedGoogle Scholar
  • 43 Roy S K, Treacy B J. Isolation and long-term culture of human preantral follicles.  Fertil Steril. 1993;  59 783-790
    PubMedGoogle Scholar
  • 44 Abir R, Franks S, Mobberley M A et al.. Mechanical isolation and in vitro growth of preantral and small antral human follicles.  Fertil Steril. 1997;  68 682-688
    CrossrefPubMedGoogle Scholar
  • 45 Gomes J E, Correia S C, Gouveia-Oliveira A et al.. Three-dimensional environments preserve extracellular matrix compartments of ovarian follicles and increase FSH-dependent growth.  Mol Reprod Dev. 1999;  54 163-172
    CrossrefPubMedGoogle Scholar
  • 46 Abir R, Fisch B, Nitke S et al.. Morphological study of fully and partially isolated early human follicles.  Fertil Steril. 2001;  75 141-146
    CrossrefPubMedGoogle Scholar
  • 47 Boland N I, Humpherson P G, Leese H J et al.. Pattern of lactate production and steroidogenesis during growth and maturation of mouse ovarian follicles in vitro.  Biol Reprod. 1993;  48 798-806
    PubMedGoogle Scholar
  • 48 Nayudu P L, Osborn S M. Factors influencing the rate of preantral and antral growth of mouse ovarian follicles in vitro.  J Reprod Fertil. 1992;  95 349-362
    PubMedGoogle Scholar
  • 49 Rowghani N M, Heise M K, McKeel D et al.. Maintenance of morphology and growth of ovarian follicles in suspension culture.  Tissue Eng. 2004;  10 545-552
    CrossrefPubMedGoogle Scholar
  • 50 Wycherley G, Downey D, Kane M T et al.. A novel follicle culture system markedly increases follicle volume, cell number and oestradiol secretion.  Reproduction. 2004;  127 669-677
    CrossrefPubMedGoogle Scholar
  • 51 Torrance C, Telfer E, Gosden R G. Quantitative study of the development of isolated mouse pre-antral follicles in collagen gel culture.  J Reprod Fertil. 1989;  87 367-374
    PubMedGoogle Scholar
  • 52 Pangas S A, Saudye H, Shea L D et al.. Novel approach for the three-dimensional culture of granulosa cell-oocyte complexes.  Tissue Eng. 2003;  9 1013-1021
    CrossrefPubMedGoogle Scholar
  • 53 Kreeger P K, Fernandes N N, Woodruff T K et al.. Regulation of mouse follicle development by follicle-stimulating hormone in a three-dimensional in vitro culture system is dependent on follicle stage and dose.  Biol Reprod. 2005;  73 942-950
    CrossrefPubMedGoogle Scholar
  • 54 Langer R, Vacanti J P. Tissue engineering.  Science. 1993;  260 920-926
    CrossrefPubMedGoogle Scholar
  • 55 Kim B S, Mooney D J. Development of biocompatible synthetic extracellular matrices for tissue engineering.  Trends Biotechnol. 1998;  16 224-230
    CrossrefPubMedGoogle Scholar
  • 56 Haug A, Larsen B. Quantitative determination of the uronic acid composition of alginates.  Acta Chem Scand. 1962;  16 1908-1918
    PubMedGoogle Scholar
  • 57 Haug A, Larsen B, Smidsrod O. Studies of the sequence of uronic acid residues in alginic acid.  Acta Chem Scand. 1967;  21 691-704
    PubMedGoogle Scholar
  • 58 Lee K Y, Mooney D J. Hydrogels for tissue engineering.  Chem Rev. 2001;  101 1869-1879
    CrossrefPubMedGoogle Scholar
  • 59 Drury J L, Mooney D J. Hydrogels for tissue engineering: scaffold design variables and applications.  Biomaterials. 2003;  24 4337-4351
    CrossrefPubMedGoogle Scholar
  • 60 Kong H J, Lee K Y, Mooney D J. Decoupling the dependence of rheological/mechanical properties of hydrogels from solids concentration.  Polym. 2002;  43 6239-6246
    CrossrefPubMedGoogle Scholar
  • 61 Kong H J, Smith M K, Mooney D J. Designing alginate hydrogels to maintain viability of immobilized cells.  Biomaterials. 2003;  24 4023-4029
    CrossrefPubMedGoogle Scholar
  • 62 Bouhadir K H, Hausman D S, Mooney D J. Synthesis of cross-linked poly(aldehyde guluronate) hydrogels.  Polymer. 1999;  40 3575-3584
    CrossrefPubMedGoogle Scholar
  • 63 Bouhadir K H, Lee K Y, Alsberg E et al.. Degradation of partially oxidized alginate and its potential application for tissue engineering.  Biotechnol Prog. 2001;  17 945-950
    CrossrefPubMedGoogle Scholar
  • 64 Rowley J A, Madlambayan G, Mooney D J. Alginate hydrogels as synthetic extracellular matrix materials.  Biomaterials. 1999;  20 45-53
    CrossrefPubMedGoogle Scholar
  • 65 Stoichet M S, Li R H, White M L et al.. Stability of hydrogels used in cell encapsulation: An in vitro comparison of alginate and agarose.  Biotechnol Bioeng. 1996;  50 374-381
    PubMedGoogle Scholar
  • 66 Li R H, Altreuter D H, Gentile F T. Transport characterization of hydrogel matrices for cell encapsulation.  Biotechnol Bioeng. 1996;  50 365-373
    PubMedGoogle Scholar
  • 67 Rodgers R J, van Wezel I L, Irving-Rodgers H F et al.. Roles of extracellular matrix in follicular development.  J Reprod Fertil Suppl. 1999;  54 343-352
    PubMedGoogle Scholar
  • 68 Rodgers R J. Extracellular matrix in the ovary.  Semin Reprod Med. 2006;  24 193-194
    Article in Thieme ConnectPubMedGoogle Scholar
  • 69 Ricciardelli C, Rodgers R J. Extracellular matrix of ovarian tumors.  Semin Reprod Med. 2006;  24 270-282
    Article in Thieme ConnectPubMedGoogle Scholar
  • 70 Monniaux D, Huet-Calderwood C, Bellego F L et al.. Integrins in the ovary.  Semin Reprod Med. 2006;  24 251-261
    Article in Thieme ConnectPubMedGoogle Scholar
  • 71 Irving-Rodgers H F, Roger J, Luck M R et al.. Extracellular matrix of the corpus luteum.  Semin Reprod Med. 2006;  24 242-250
    Article in Thieme ConnectPubMedGoogle Scholar
  • 72 Curry Jr T E, Smith M F. Impact of extracellular matrix remodeling on ovulation and the folliculo-luteal transition.  Semin Reprod Med. 2006;  24 228-241
    Article in Thieme ConnectPubMedGoogle Scholar
  • 73 Russell D L, Salustri A. Extracellular matrix of the cumulus-oocyte complex.  Semin Reprod Med. 2006;  24 217-227
    Article in Thieme ConnectPubMedGoogle Scholar
  • 74 Lutolf M P, Hubbell J A. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering.  Nat Biotechnol. 2005;  23 47-55
    CrossrefPubMedGoogle Scholar
  • 75 Shin H, Jo S, Mikos A G. Biomimetic materials for tissue engineering.  Biomaterials. 2003;  24 4353-4364
    CrossrefPubMedGoogle Scholar
  • 76 Silva E A, Mooney D J. Synthetic extracellular matrices for tissue engineering and regeneration.  Curr Top Dev Biol. 2004;  64 181-205
    CrossrefPubMedGoogle Scholar
  • 77 Hubbell J A. Materials as morphogenetic guides in tissue engineering.  Curr Opin Biotechnol. 2003;  14 551-558
    CrossrefPubMedGoogle Scholar
  • 78 Liu W F, Chen C S. Engineering biomaterials to control cell function.  Materials Today. 2005;  8 28-35
    PubMedGoogle Scholar
  • 79 Discher D E, Janmey P, Wang Y L. Tissue cells feel and respond to the stiffness of their substrate.  Science. 2005;  310 1139-1143
    CrossrefPubMedGoogle Scholar
  • 80 Brandl F, Sommer F, Goepferich A. Rational design of hydrogels for tissue engineering: Impact of physical factors on cell behavior.  Biomaterials. 2007;  28 134-146
    PubMedGoogle Scholar
  • 81 Paszek M J, Weaver V M. The tension mounts: mechanics meets morphogenesis and malignancy.  J Mammary Gland Biol Neoplasia. 2004;  9 325-342
    CrossrefPubMedGoogle Scholar
  • 82 Marti A, Feng Z, Altermatt H J et al.. Milk accumulation triggers apoptosis of mammary epithelial cells.  Eur J Cell Biol. 1997;  73 158-165
    PubMedGoogle Scholar
  • 83 Paszek M J, Zahir N, Johnson K R et al.. Tensional homeostasis and the malignant phenotype.  Cancer Cell. 2005;  8 241-254
    CrossrefPubMedGoogle Scholar
  • 84 Oster G F, Murray J D, Harris A K. Mechanical aspects of mesenchymal morphogenesis.  J Embryol Exp Morphol. 1983;  78 83-125
    PubMedGoogle Scholar
  • 85 Trinkaus J P. Cells into organs: The forces that shape the embryo. 2nd ed. Englewood Cliffs, NJ; Prentice Hall College Division 1984
    Google Scholar
  • 86 Farge E. Mechanical induction of Twist in the Drosophila foregut/stomodeal primordium.  Curr Biol. 2003;  13 1365-1377
    CrossrefPubMedGoogle Scholar
  • 87 Ingber D E. Mechanobiology and diseases of mechanotransduction.  Ann Med. 2003;  35 564-577
    CrossrefPubMedGoogle Scholar
  • 88 Janmey P A, Weitz D A. Dealing with mechanics: mechanisms of force transduction in cells.  Trends Biochem Sci. 2004;  29 364-370
    CrossrefPubMedGoogle Scholar
  • 89 Katsumi A, Orr A W, Tzima E et al.. Integrins in mechanotransduction.  J Biol Chem. 2004;  279 12001-12004
    PubMedGoogle Scholar
  • 90 Davies P F. Flow-mediated endothelial mechanotransduction.  Physiol Rev. 1995;  75 519-560
    PubMedGoogle Scholar
  • 91 Chen C S, Tan J, Tien J. Mechanotransduction at cell-matrix and cell-cell contacts.  Annu Rev Biomed Eng. 2004;  6 275-302
    CrossrefPubMedGoogle Scholar
  • 92 Epstein N D, Davis J S. Sensing stretch is fundamental.  Cell. 2003;  112 147-150
    CrossrefPubMedGoogle Scholar
  • 93 Gillespie P G, Walker R G. Molecular basis of mechanosensory transduction.  Nature. 2001;  413 194-202
    CrossrefPubMedGoogle Scholar
  • 94 Blount P. Molecular mechanisms of mechanosensation: big lessons from small cells.  Neuron. 2003;  37 731-734
    CrossrefPubMedGoogle Scholar
  • 95 Torday J S, Rehan V K. Mechanotransduction determines the structure and function of lung and bone: a theoretical model for the pathophysiology of chronic disease.  Cell Biochem Biophys. 2003;  37 235-246
    PubMedGoogle Scholar
  • 96 Alenghat F J, Ingber D E. Mechanotransduction: all signals point to cytoskeleton, matrix, and integrins. Sci STKE 2002 2002 PE6
    Google Scholar
  • 97 Hamill O P, Martinac B. Molecular basis of mechanotransduction in living cells.  Physiol Rev. 2001;  81 685-740
    PubMedGoogle Scholar
  • 98 Gudi S R, Clark C B, Frangos J A. Fluid flow rapidly activates G proteins in human endothelial cells. Involvement of G proteins in mechanochemical signal transduction.  Circ Res. 1996;  79 834-839
    PubMedGoogle Scholar
  • 99 Shyy J Y, Chien S. Role of integrins in endothelial mechanosensing of shear stress.  Circ Res. 2002;  91 769-775
    CrossrefPubMedGoogle Scholar
  • 100 Dull R O, Tarbell J M, Davies P F. Mechanisms of flow-mediated signal transduction in endothelial cells: kinetics of ATP surface concentrations.  J Vasc Res. 1992;  29 410-419
    PubMedGoogle Scholar
  • 101 Ali M H, Schumacker P T. Endothelial responses to mechanical stress: where is the mechanosensor?.  Crit Care Med. 2002;  30 S198-S206
    CrossrefPubMedGoogle Scholar
  • 102 Tschumperlin D J, Dai G, Maly I V et al.. Mechanotransduction through growth-factor shedding into the extracellular space.  Nature. 2004;  429 83-86
    PubMedGoogle Scholar
  • 103 Bryant S J, Chowdhury T T, Lee D A et al.. Crosslinking density influences chondrocyte metabolism in dynamically loaded photocrosslinked poly(ethylene glycol) hydrogels.  Ann Biomed Eng. 2004;  32 407-417
    CrossrefPubMedGoogle Scholar
  • 104 Bryant S J, Durand K L, Anseth K S. Manipulations in hydrogel chemistry control photoencapsulated chondrocyte behavior and their extracellular matrix production.  J Biomed Mater Res A. 2003;  67 1430-1436
    PubMedGoogle Scholar
  • 105 Bryant S J, Anseth K S. Hydrogel properties influence ECM production by chondrocytes photoencapsulated in poly(ethylene glycol) hydrogels.  J Biomed Mater Res. 2002;  59 63-72
    PubMedGoogle Scholar
  • 106 Engler A J, Sen S, Sweeney H L et al.. Matrix elasticity directs stem cell lineage specification.  Cell. 2006;  126 677-689
    CrossrefPubMedGoogle Scholar
  • 107 Ries L AG, Percy C L, Bunin B R. Introduction. In: Ries LAG, Smith MA, Gurney JG et al. Cancer Incidence and Survival among Children and Adolescents: United States SEER Program 1975-1995. NIH Publication no. 99-4649. Bethesda, MD; National Cancer Institute 1999: 1-15
    Google Scholar
  • 108 Blatt J. Pregnancy outcome in long-term survivors of childhood cancer.  Med Pediatr Oncol. 1999;  33 29-33
    CrossrefPubMedGoogle Scholar
  • 109 Weintraub M, Gross E, Kadari A et al.. Should ovarian cryopreservation be offered to girls with cancer.  Pediatr Blood Cancer. 2007;  48 4-9
    CrossrefPubMedGoogle Scholar
  • 110 Maltaris T, Boehm D, Dittrich R et al.. Reproduction beyond cancer: a message of hope for young women.  Gynecol Oncol. 2006;  103 1109-1121
    CrossrefPubMedGoogle Scholar
  • 111 Maltaris T, Seufert R, Fischl F et al.. The effect of cancer treatment on female fertility and strategies for preserving fertility.  Eur J Obstet Gynecol Reprod Biol. 2007;  130 148-155
    CrossrefPubMedGoogle Scholar
  • 112 Donnez J, Martinez-Madrid B, Jadoul P et al.. Ovarian tissue cryopreservation and transplantation: a review.  Hum Reprod Update. 2006;  12 519-535
    CrossrefPubMedGoogle Scholar
  • 113 Nieman C L, Kazer R, Brannigan R E et al.. Cancer survivors and infertility: a review of a new problem and novel answers.  J Support Oncol. 2006;  4 171-178
    PubMedGoogle Scholar
  • 114 Meirow D, Levron J, Eldar-Geva T et al.. Pregnancy after transplantation of cryopreserved ovarian tissue in a patient with ovarian failure after chemotherapy.  N Engl J Med. 2005;  353 318-321
    CrossrefPubMedGoogle Scholar
  • 115 Donnez J, Dolmans M M, Demylle D et al.. Livebirth after orthotopic transplantation of cryopreserved ovarian tissue.  Lancet. 2004;  364 1405-1410
    CrossrefPubMedGoogle Scholar
  • 116 Fabbri R. Cryopreservation of human oocytes and ovarian tissue.  Cell Tissue Bank. 2006;  7 113-122
    CrossrefPubMedGoogle Scholar
  • 117 Dolmans M M, Michaux N, Camboni A et al.. Evaluation of Liberase, a purified enzyme blend, for the isolation of human primordial and primary ovarian follicles.  Hum Reprod. 2006;  21 413-420
    CrossrefPubMedGoogle Scholar
  • 118 The Practice Committee of the American Society for Reproductive Medicine . Ovarian hyperstimulation syndrome.  Fertil Steril. 2006;  86(suppl 5) S178-S183
    PubMedGoogle Scholar
  • 119 Abir R, Roizman P, Fisch B et al.. Pilot study of isolated early human follicles cultured in collagen gels for 24 hours.  Hum Reprod. 1999;  14 1299-1301
    CrossrefPubMedGoogle Scholar
  • 120 Vitt U A, Nayudu P L, Rose U M et al.. Embryonic development after follicle culture is influenced by follicle-stimulating hormone isoelectric point range.  Biol Reprod. 2001;  65 1542-1547
    CrossrefPubMedGoogle Scholar
  • 121 Spears N, Boland N I, Murray A A et al.. Mouse oocytes derived from in vitro grown primary ovarian follicles are fertile.  Hum Reprod. 1994;  9 527-532
    PubMedGoogle Scholar
  • 122 Heise M, Koepsel R, Russell A J et al.. Calcium alginate microencapsulation of ovarian follicles impacts FSH delivery and follicle morphology.  Reprod Biol Endocrinol. 2005;  3 47
    CrossrefPubMedGoogle Scholar

Teresa K WoodruffPh.D. 

Department of Obstetrics and Gynecology, The Feinberg School of Medicine

Northwestern University, Chicago, IL 60611

Email: tkw@northwestern.edu

      >