GPR56 is essential for testis development and male fertility in mice

Developmental Dynamics

Volumn 239, Issue 12, 2010, Pages 3358-3367

  Chen, Guangchun ^a   Yang, Liquan ^a   Begum, Shahinoor ^b   Xu, Lei ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Fertility; GPR56; Polarity; Seminiferous tubules; Testis

Indexed keywords

G PROTEIN COUPLED RECEPTOR; PROTEIN GPR56; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION; MALE; MALE FERTILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEMINIFEROUS TUBULE; SUBFERTILITY; TESTIS DEVELOPMENT;

ANIMALS; CELLS, CULTURED; FERTILITY; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MICE; MICE, MUTANT STRAINS; RECEPTORS, G-PROTEIN-COUPLED; SEMINIFEROUS TUBULES; SERTOLI CELLS; TESTIS;

MAMMALIA; MUS;

EID: 78649704283     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22468     Document Type: Article

References (57)

1. Andrew DJ, Ewald AJ. 2010. Morphogenesis of epithelial tubes: insights into tube formation, elongation, and elaboration. Dev Biol 341: 34-55.
2. Barrionuevo F, Bagheri-Fam S, Klattig J, Kist R, Taketo MM, Englert C, Scherer G. 2006. Homozygous inactivation of Sox9 causes complete XY sex reversal in mice. Biol Reprod 74: 195-201.
3. Behringer RR, Finegold MJ, Cate RL. 1994. Mullerian-inhibiting substance function during mammalian sexual development. Cell 79: 415-425.
4. Bitgood MJ, Shen L, McMahon AP. 1996. Sertoli cell signaling by Desert hedgehog regulates the male germline. Curr Biol 6: 298-304.
5. Brennan J, Capel B. 2004. One tissue, two fates: molecular genetic events that underlie testis versus ovary development. Nat Rev Genet 5: 509-521.
6. Brennan J, Tilmann C, Capel B. 2003. Pdgfr-alpha mediates testis cord organization and fetal Leydig cell development in the XY gonad. Genes Dev 17: 800-810.
7. Bryant DM, Mostov KE. 2008. From cells to organs: building polarized tissue. Nat Rev Mol Cell Biol 9: 887-901.
8. Buehr M, Gu S, McLaren A. 1993. Mesonephric contribution to testis differentiation in the fetal mouse. Development 117: 273-281.
9. Capel B. 2000. The battle of the sexes. Mech Dev 92: 89-103.
10. Clark AM, Garland KK, Russell LD. 2000. Desert hedgehog (Dhh) gene is required in the mouse testis for formation of adult-type Leydig cells and normal development of peritubular cells and seminiferous tubules. Biol Reprod 63: 1825-1838.
11. Collinet C, Stoter M, Bradshaw CR, Samusik N, Rink JC, Kenski D, Habermann B, Buchholz F, Henschel R, Mueller MS, Nagel WE, Fava E, Kalaidzidis Y, Zerial M. 2010. Systems survey of endocytosis by multiparametric image analysis. Nature 464: 243-249.
12. Colvin JS, Green RP, Schmahl J, Capel B, Ornitz DM. 2001. Male-to-female sex reversal in mice lacking fibroblast growth factor 9. Cell 104: 875-889.
13. Combes AN, Lesieur E, Harley VR, Sinclair AH, Little MH, Wilhelm D, Koopman P. 2009. Three-dimensional visualization of testis cord morphogenesis, a novel tubulogenic mechanism in development. Dev Dyn 238: 1033-1041.
14. Curtin JA, Quint E, Tsipouri V, Arkell RM, Cattanach B, Copp AJ, Henderson DJ, Spurr N, Stanier P, Fisher EM, Nolan PM, Steel KP, Brown SD, Gray IC, Murdoch JN. 2003. Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Curr Biol 13: 1129-1133.
15. Gonczy P. 2008. Mechanisms of asymmetric cell division: flies and worms pave the way. Nat Rev Mol Cell Biol 9: 355- 366.
16. Gumbiner BM. 2005. Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol 6: 622-634.
17. Hadley MA, Byers SW, Suarez-Quian CA, Kleinman HK, Dym M. 1985. Extracellular matrix regulates Sertoli cell differentiation, testicular cord formation, and germ cell development in vitro. J Cell Biol 101: 1511-1522.
18. Haider SG, Talati J, Servos G. 1999. Ultrastructure of peritubular tissue in association with tubular hyalinization in human testis. Tissue Cell 31: 90-98.
19. Iguchi T, Sakata K, Yoshizaki K, Tago K, Mizuno N, Itoh H. 2008. Orphan G protein-coupled receptor GPR56 regulates neural progenitor cell migration via a G alpha 12/13 and Rho pathway. J Biol Chem 283: 14469-14478.
20. Jones C, Chen P. 2007. Planar cell polarity signaling in vertebrates. Bioessays 29: 120-132.
21. Kahsai TZ, Enders GC, Gunwar S, Brunmark C, Wieslander J, Kalluri R, Zhou J, Noelken ME, Hudson BG. 1997. Seminiferous tubule basement membrane. Composition and organization of type IV collagen chains, and the linkage of alpha3(IV) and alpha5(IV) chains. J Biol Chem 272: 17023-17032.
22. Koirala S, Jin Z, Piao X, Corfas G. 2009. GPR56-regulated granule cell adhesion is essential for rostral cerebellar development. J Neurosci 29: 7439-7449.
23. Kwakkenbos MJ, Pouwels W, Matmati M, Stacey M, Lin HH, Gordon S, van Lier RA, Hamann J. 2005. Expression of the largest CD97 and EMR2 isoforms on leukocytes facilitates a specific interaction with chondroitin sulfate on B cells. J Leukoc Biol 77: 112-119.
24. Langenhan T, Promel S, Mestek L, Esmaeili B, Waller-Evans H, Hennig C, Kohara Y, Avery L, Vakonakis I, Schnabel R, Russ AP. 2009. Latrophilin signaling links anterior-posterior tissue polarity and oriented cell divisions in the C. elegans embryo. Dev Cell 17: 494-504.
25. Li S, Jin Z, Koirala S, Bu L, Xu L, Hynes RO, Walsh CA, Corfas G, Piao X. 2008. GPR56 regulates pial basement membrane integrity and cortical lamination. J Neurosci 28: 5817-5826.
26. Little KD, Hemler ME, Stipp CS. 2004. Dynamic regulation of a GPCR-tetraspanin-G protein complex on intact cells: central role of CD81 in facilitating GPR56-Galpha q/11 association. Mol Biol Cell 15: 2375-2387.
27. Martineau J, Nordqvist K, Tilmann C, Lovell-Badge R, Capel B. 1997. Male-specific cell migration into the developing gonad. Curr Biol 7: 958-968.
28. McLaren A. 1991. Development of the mammalian gonad: the fate of the supporting cell lineage. Bioessays 13: 151-156.
29. Mellman I, Nelson WJ. 2008. Coordinated protein sorting, targeting and distribution in polarized cells. Nat Rev Mol Cell Biol 9: 833-845.
30. Miner JH, Yurchenco PD. 2004. Laminin functions in tissue morphogenesis. Annu Rev Cell Dev Biol 20: 255-284.
31. Morais da Silva S, Hacker A, Harley V, Goodfellow P, Swain A, Lovell-Badge R. 1996. Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat Genet 14: 62-68.
32. Nejsum LN, Nelson WJ. 2009. Epithelial cell surface polarity: the early steps. Front Biosci 14: 1088-1098.
33. O'Shaughnessy PJ, Morris ID, Huhtaniemi I, Baker PJ, Abel MH. 2009. Role of androgen and gonadotrophins in the development and function of the Sertoli cells and Leydig cells: data from mutant and genetically modified mice. Mol Cell Endocrinol 306: 2-8.
34. Piao X, Hill RS, Bodell A, Chang BS, Basel-Vanagaite L, Straussberg R, Dobyns WB, Qasrawi B, Winter RM, Innes AM, Voit T, Ross ME, Michaud JL, Descarie JC, Barkovich AJ, Walsh CA. 2004. G protein-coupled receptor-dependent development of human frontal cortex. Science 303: 2033-2036.
35. Pierucci-Alves F, Clark AM, Russell LD. 2001. A developmental study of the Desert hedgehog-null mouse testis. Biol Reprod 65: 1392-1402.
36. Rodriguez-Boulan E, Kreitzer G, Musch A. 2005. Organization of vesicular trafficking in epithelia. Nat Rev Mol Cell Biol 6: 233-247.
37. Salomon F, Hedinger CE. 1982. Abnormal basement membrane structures of seminiferous tubules in infertile men. Lab Invest 47: 543-554.
38. Sharpe RM, McKinnell C, Kivlin C, Fisher JS. 2003. Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 125: 769-784.
39. Shima JE, McLean DJ, McCarrey JR, Griswold MD. 2004. The murine testicular transcriptome: characterizing gene expression in the testis during the progression of spermatogenesis. Biol Reprod 71: 319-330.
40. Soriano P. 1994. Abnormal kidney development and hematological disorders in PDGF beta-receptor mutant mice. Genes Dev 8: 1888-1896.
41. Stacey M, Chang GW, Davies JQ, Kwakkenbos MJ, Sanderson RD, Hamann J, Gordon S, Lin HH. 2003. The epidermal growth factor-like domains of the human EMR2 receptor mediate cell attachment through chondroitin sulfate glycosaminoglycans. Blood 102: 2916-2924.
42. Tilmann C, Capel B. 1999. Mesonephric cell migration induces testis cord formation and Sertoli cell differentiation in the mammalian gonad. Development 126: 2883-2890.
43. Tung PS, Fritz IB. 1990. Characterization of rat testicular peritubular myoid cells in culture: alpha-smooth muscle isoactin is a specific differentiation marker. Biol Reprod 42: 351-365.
44. Tung PS, Skinner MK, Fritz IB. 1984a. Cooperativity between Sertoli cells and peritubular myoid cells in the formation of the basal lamina in the seminiferous tubule. Ann N Y Acad Sci 438: 435-446.
45. Tung PS, Skinner MK, Fritz IB. 1984b. Fibronectin synthesis is a marker for peritubular cell contaminants in Sertoli cell-enriched cultures. Biol Reprod 30: 199-211.
46. Wang D, Enders GC. 1996. Expression of a specific mouse germ cell nuclear antigen (GCNA1) by early embryonic testicular teratoma cells in 129/Sv-Sl/+ mice. Cancer Lett 100: 31-36.
47. Wang T, Ward Y, Tian L, Lake R, Guedez L, Stetler-Stevenson WG, Kelly K. 2005. CD97, an adhesion receptor on inflammatory cells, stimulates angiogenesis through binding integrin counterreceptors on endothelial cells. Blood 105: 2836-2844.
48. Wang Y, Nathans J. 2007. Tissue/planar cell polarity in vertebrates: new insights and new questions. Development 134: 647-658.
49. Whittaker CA, Bergeron KF, Whittle J, Brandhorst BP, Burke RD, Hynes RO. 2006. The echinoderm adhesome. Dev Biol 300: 252-266.
50. Wilhelm D, Koopman P. 2006. The makings of maleness: towards an integrated view of male sexual development. Nat Rev Genet 7: 620-631.
51. Wilhelm D, Palmer S, Koopman P. 2007. Sex determination and gonadal development in mammals. Physiol Rev 87: 1-28.
52. Xu L, Begum S, Hearn JD, Hynes RO. 2006. GPR56, an atypical G protein-coupled receptor, binds tissue transglutaminase, TG2, and inhibits melanoma tumor growth and metastasis. Proc Natl Acad Sci U S A 103: 9023-9028.
53. Yagi H, Tokano H, Maeda M, Takabayashi T, Nagano T, Kiyama H, Fujieda S, Kitamura K, Sato M. 2007. Vlgr1 is required for proper stereocilia maturation of cochlear hair cells. Genes Cells 12: 235-250.
54. Yao HH, Whoriskey W, Capel B. 2002. Desert Hedgehog/Patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes Dev 16: 1433-1440.
55. Yona S, Lin HH, Siu WO, Gordon S, Stacey M. 2008. Adhesion-GPCRs: emerging roles for novel receptors. Trends Biochem Sci 33: 491-500.
56. Yu W, Datta A, Leroy P, O'Brien LE, Mak G, Jou TS, Matlin KS, Mostov KE, Zegers MM. 2005. Beta1-integrin orients epithelial polarity via Rac1 and laminin. Mol Biol Cell 16: 433-445.
57. Zallen JA, Blankenship JT. 2008. Multicellular dynamics during epithelial elongation. Semin Cell Dev Biol 19: 263-270.