2,5-Hexanedione-Induced Testicular Injury

Annual Review of Pharmacology and Toxicology

Volumn 43, Issue , 2003, Pages 125-147

  Boekelheide, Kim ^a   Fleming, Shawna L ^a   Allio, Theresa ^a   Embree Ku, Michelle E ^a   Hall, Susan J ^a   Johnson, Kamin J ^a   Kwon, Eun Ji ^a   Patel, Sutchin R ^a   Rasoulpour, Reza J ^a   Schoenfeld, Heidi A ^a   Thompson, Stephanie ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Apoptosis; Microtubule; Sertoli cell; Testis; Toxicant

Indexed keywords

ACETONYLACETONE; 2,5-HEXANEDIONE; ALKANONE; CROSS LINKING REAGENT;

APOPTOSIS; CELL FUNCTION; CELL MATURATION; DATA BASE; GERM CELL; HUMAN; MALE; MICROTUBULE; MOLECULAR BIOLOGY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SERTOLI CELL; TESTIS INJURY; ANIMAL; CHEMICALLY INDUCED DISORDER; DISEASE MODEL; DRUG EFFECT; PATHOLOGY; POLLUTANT; TESTIS; TESTIS DISEASE;

ANIMALS; CROSS-LINKING REAGENTS; DISEASE MODELS, ANIMAL; ENVIRONMENTAL POLLUTANTS; HEXANONES; HUMANS; MALE; TESTICULAR DISEASES; TESTIS;

EID: 0041350371     PISSN: 03621642     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.pharmtox.43.100901.135930     Document Type: Review

References (119)

1. Ikeda M, Kasahara M. 1986. n-Hexane and benzene contents in gasoline for industrial purpose. Ind. Health 24:63-66
2. DiVincenzo GD, Kaplan CJ, Dedinas J. 1976. Characterization of the metabolites of methyl n-butyl ketone, methyl isobutyl ketone, and methyl ethyl ketone in guinea pig serum and their clearance. Toxicol. Appl. Pharmacol. 36:511-22
3. 14C-labeled methyl n-butyl ketone in the rat. Toxicol. Appl. Pharmacol. 41:547-60
4. Graham DG, Anthony DC, Boekelheide K, Maschmann NA, Richards RG, et al. 1982. Studies of the molecular pathogenesis of hexane neuropathy. II. Evidence that pyrrole derivatization of lysy1 residues leads to protein crosslinking. Toxicol. Appl. Pharmacol. 64:415-22
5. DeCaprio AP, Olajas EJ, Weber P. 1982. Covalent binding of a neurotoxic n-hexane metabolite: conversion of primary amines to substitituted pyrrole adducts by 2,5-hexanedione. Toxicol. Appl. Pharmacol. 65:440-50
6. DeCaprio AP, Briggs RG, Jackowski SJ, Kim JC. 1988. Comparative neurotoxicity and pyrrole-forming potential of 2,5-hexanedione and perdeuterio-2,5-hexanedione in the rat. Toxicol. Appl. Pharmacol. 92:75-85
7. Genter MB, Szakal-Quin G, Anderson CW, Anthony DC, Graham DG. 1987. Evidence that pyrrole formation is a pathogenetic step in gamma-diketone neuropathy. Toxicol. Appl. Pharmacol. 87:351-62
8. Sayre LM, Shearson CM, Wongmongkolrit T, Medori R, Gambetti P. 1986. Structural basis of gamma-diketone neurotoxicity: non-neurotoxicity of 3,3-dimethyl-2,5-hexanedione, a gamma-diketone incapable of pyrrole formation. Toxicol. Appl. Pharmacol. 84:36-44
9. Amamath V, Valentine WM, Amamath K, Eng MA, Graham DG. 1994. The mechanism of nucleophilic substitiution of alkylpyrroles in the presence of oxygen. Chem. Res. Toxicol. 7:56-61
10. Zhu M, Spink DC, Yan B, Bank S, DeCaprio AP. 1994. Formation and structure of crosslinking and monomeric pyrrole autoxidation products in 2,5-hexanedione-treated amino acids, peptides, and protein. Chem. Res. Toxicol. 7:551-58
11. Korobkin R, Asbury AK, Sumner AJ, Nielsen SL. 1975. Glue sniffing neuropathy. Arch. Neurol. 32:158-62
12. Schaumburg HH, Spencer PS. 1976. Degeneration in central and peripheral nervous systems produced by pure n-hexane: an experimental study. Brain 99:183-92
13. Spencer PS, Schaumberg HS, Sabri MI, Veronesi B, DiVincenzo GD. 1980. The enlarging view of hexacarbon neurotoxicity. CRC Crit. Rev. Toxicol. 7:278-356
14. Allen N, Mendell JR, Billmaier DJ, Fontaine RE, O'Neill J. 1975. Toxic polyneuropathy due to methyl n-butyl ketone. Arch. Neurol. 32:209-18
15. Graham DG, Anthony DC, Szakal-Quin G, Gottfried MR, Boekelheide K. 1985. Covalent crosslinking of neurofilaments in the pathogenesis of n-hexane neuropathy. Neurotoxicology 6:55-63
16. LoPachin RM, Lehning EJ. 1997. The relevance of axonal swellings and atrophy to gamma-diketone neurotoxicity: a forum position paper. Neurotoxicology 18:7-22
17. Anthony DC. 1997. Specificity of neurofilament swellings and axonal atrophy: commentary on forum position paper. Neurotoxicology 18:23-24
18. DeCaprio AP. 1997. Axonal swellings vs atrophy: what is the relevance to gamma-diketone peripheral neuropathy? Neurotoxicology 18:25-27
19. Graham DG. 1997. Protein crosslinking correlates with axonal atrophy, swelling and degeneration in gamma-diketone neuropathy: commentary on forum position paper. Neurotoxicology 18:29-30
20. Sayre LM, Gambetti P. 1997. Mechanistic importance of axonal atrophy and swelling in gamma-diketone axonopathy: commentary on forum position paper. Neurotoxicology 18:31-32
21. Sickles DW. 1997. Neurofilamentous swellings and axonal atrophy are of unclear significance to diketone toxicity: commentary on forum position paper. Neurotoxicology 18:33-36
22. Krasavage WJ, O'Donoghue JL, Terhaar CJ. 1980. The relative neurotoxicity of methyl n-butyl ketone, n-hexane and their metabolites. Toxicol. Appl. Pharmacol. 52:433-41
23. Chapin RE, Norton RM, Popp JA, Bus JS. 1982. The effects of 2,5-hexanedione on reproductive hormones and testicular enzyme activities in the F-344 rat. Toxicol. Appl. Pharmacol. 62:262-72
24. Chapin RE, Morgan KT, Bus JS. 1983. The morphogenesis of testicular degeneration induced in rats by orally administered 2,5-hexanedione. Exp. Mol. Pathol. 38:149-69
25. Boekelheide K. 1987. 2,5-Hexanedione alters microtubule assembly. I. Testicular atrophy, not nervous system toxicity, correlates with enhanced tubulin polymerization. Toxicol. Appl. Pharmacol. 88:370-82
26. Boekelheide K. 1988. Rat testis during 2,5-hexanedione intoxication and recovery. II. Dynamics of pyrrole reactivity, tubulin content, and microtubule assembly. Toxicol. Appl. Pharmacol. 92:28-33
27. Richburg JH, Redenbach DM, Boekelheide K. 1994. Seminiferous tubule fluid secretion is a Sertoli cell microtubule-dependent process inhibited by 2,5-hexanedione exposure. Toxicol. Appl. Pharmacol. 128:302-9
28. Boekelheide K. 1988. Rat testis during 2,5-hexanedione intoxication and recovery. I. Dose response and the reversibity of germ cell loss. Toxicol. Appl. Pharmacol. 92:18-27
29. Rosiepen G, Chapin RE, Weinbauer GF. 1995. The duration of the cycle of the seminiferous epithelium is altered by administration of 2,5-hexanedione in the adult Sprague-Dawley rat. J. Androl. 16:127-35
30. Boekelheide K, Hall SJ. 1991. 2,5-Hexanedione exposure in the rat results in long-term testicular atrophy despite the presence of residual spermatogonia. J. Androl. 12:18-26
31. Boekelheide K, Eveleth J. 1988. The rate of 2,5-hexanedione intoxication, not total dose, determines the extent of testicular injury and altered microtubule assembly in the rat. Toxicol. Appl. Pharmacol. 94:76-83
32. Anthony DC, Boekelheide K, Graham DG. 1983. The effect of 3,4-dimethyl substitution on the neurotoxicity of 2,5-hexanedione. I. Accelerated clinical neuropathy is accompanied by more proximal axonal swellings. Toxicol. Appl. Pharmacol. 71:362-71
33. Neely MD, Boekelheide K. 1988. Sertoli cell processes have axoplasmic features: an ordered microtubule distribution and an abundant high molecular weight microtubule-associated protein (cytoplasmic dynein). J. Cell Biol. 107:1767-76
34. Dustin P. 1984. Microtubules. Berlin: Springer-Verlag. 482 pp. 2nd ed.
35. Nogales E. 2000. Structural insights into microtubule function. Annu. Rev. Biochem. 69:277-302
36. Walczak CE. 2000. Microtubule dynamics and tubulin interacting proteins. Curr. Opin. Cell Biol. 12:52-56
37. Walker RA, O'Brien ET, Pryer NK, Sobeiro MF, Voter WA, et al. 1988. Dynamic instability of individual microtubules analysed by video light microscopy: rate constants and transition frequencies. J. Cell Biol. 107:1437-48
38. Nachtman JP, Couri D. 1979. Studies on hexane 2,5-dione neurotoxicity: no effect on microtubular properties. Toxicol. Appl. Pharmacol. 48:A54(Abstr.)
39. Selkoe DJ, Luckenbill-Edds L, Shelanski ML. 1978. Effects of neurotoxic industrial solvents on cultured neuroblastoma cells: methyl n-butyl ketone, n-hexane and derivatives. J. Neuropathol. Exp. Neurol. 37:768-89
40. Boekelheide K. 1987. 2,5-Hexanedione alters microtubule assembly. II. Enhanced polymerization of crosslinked tubulin. Toxicol. Appl. Pharmacol. 88:383-96
41. Sioussat T, Boekelheide K. 1989. Selection of a nucleation-promoting element following chemical modification of tubulin. Biochemistry 28:4435-43
42. Sioussat TM, Miller FJ, Boekelheide K. 1990. 2,5-Hexanedione-treated tubulin microinjected into sea urchin zygotes induces mitotic abnormalities. Toxicol. Appl. Pharmacol. 104:36-46
43. Meads T, Schroer TA. 1995. Polarity and nucleation of microtubules in polarized epithelial cells. Cell Motil. Cytoskelet. 32:273-88
44. Rindler MJ, Ivanov IE, Sabatini DD. 1987. Microtubule-acting drugs lead to the nonpolarized delivery of the influenza hemagglutinin to the cell surface of polarized Madin-Darby canine kidney cells. J. Cell Biol. 104:231-41
45. Redenbach DM, Boekelheide K. 1994. Microtubules are oriented with their minus-ends directed apically before tight junction formation in rat Sertoli cells. Eur. J. Cell Biol. 65:246-57
46. Redenbach DM, Vogl AW. 1991. Microtubule polarity in Sertoli cells: a model for microtubule-based spermatid transport. Eur. J. Cell Biol. 54:277-90
47. Vogl AW, Weis M, Pfeiffer DC. 1995. The perinuclear centriole-containing centrosome is not the major microtubule organizing center in Sertoli cells. Eur. J. Cell Biol. 66:165-79
48. Sablin EP. 2000. Kinesins and microtubules: their structures and motor mechanisms. Curr. Opin. Cell Biol. 12:35-41
49. Neely MD, Erickson HP, Boekelheide K. 1990. HMW-2, the Sertoli cell cytoplasmic dynein from rat testis, is a dimer composed of nearly identical subunits. J. Biol. Chem. 265:8691-98
50. Hall ES, Eveleth J, Jiang C, Redenbach DM, Boekelheide K. 1992. Distribution of the microtubule-dependent motors cytoplasmic dynein and kinesin in rat testis. Biol. Reprod. 46:817-28
51. Redenbach DM, Hall ES, Boekelheide K. 1995. Distribution of Sertoli cell microtubules, microtubule-dependent motors, and the Golgi apparatus before and after tight junction formation in developing rat testis. Microsc. Res. Tech. 32:504-19
52. Redenbach DM, Boekelheide K, Vogl AW. 1992. Binding between mammalian spermatid-ectoplasmic specialization complexes and microtubules. Eur. J. Cell Biol. 59:433-48
53. Beach SF, Vogl AW. 1999. Spermatid translocation in the rat seminiferous epithelium: coupling membrane trafficking machinery to a junction plaque. Biol. Reprod. 60:1036-46
54. Vogl AW, Pfeiffer DC, Mulholland D, Kimel G, Guttman J. 2000. Unique and multifunctional adhesion junctions in the testis: ectoplasmic specializations. Arch. Histol. Cytol. 63:1-15
55. Guttman JA, Kimel GH, Vogl AW. 2000. Dynein and plus-end microtubule-dependent motors are associated with specialized Sertoli cell junction plaques (ectoplasmic specializations). J. Cell Sci. 113:167-76
56. Prahlad V, Helfand BT, Langford GM, Vale RD, Goldman RD. 2000. Fast transport of neurofilament protein along microtubules in squid axoplasm. J. Cell Sci. 113:3939-46
57. Johnson KJ, Hall ES, Boekelheide K. 1996. Kinesin localizes to the trans-Golgi network regardless of microtubule organization. Eur. J. Cell Biol. 69:276-87
58. Hall ES, Hall SJ, Boekelheide K. 1995. 2,5-Hexanedione exposure alters microtubule motor distribution in adult rat testis. Fundam. Appl. Toxicol. 24:173-82
59. Redenbach DM, Richburg JH, Boekelheide K. 1994. Microtubules with altered assembly kinetics have a decreased rate of kinesin-based transport. Cell Motil. Cytoskelet. 27:79-87
60. Johnson KJ, Hall ES, Boekelheide K. 1991. 2,5-Hexanedione exposure alters the rat Sertoli cell cytoskeleton. I. Microtubules and seminiferous tubule fluid secretion. Toxicol. Appl. Pharmacol. 111: 432-42
61. Achler C, Filmer D, Merte C, Drenckhahn D. 1989. Role of microtubules in polarized delivery of apical membrane proteins to the brush border of the intestinal epithelium. J. Cell Biol. 109:179-89
62. Van der Sluijs P, Bennett MK, Antony C, Simons K, Kreis TE. 1990. Binding of exocytic vesicles from MDCK cells to microtubales in vitro. J. Cell Sci. 95:545-53
63. Allan DJ, Harmon BV, Roberts SA. 1992. Spermatogonial apoptosis has three morphologically recognizable phases and shows no circadian rhythm during normal spermatogenesis in the rat. Cell Prolif. 25:241-50
64. Hermo L, Clermont Y. 1976. Light cells within the limiting membrane of rat seminiferous tubules. Am. J. Anat. 145:467-83
65. Huckins C. 1978. The morphology and kinetics of spermatogonial degeneration in normal adult rats: an analysis using simplified classification of germinal epithelium. Anat. Rec. 190:905-26
66. Hasegawa M, Wilson G, Russell LD, Meistrich ML. 1997. Radiation-induced cell death in the mouse testis: relationship to apoptosis. Radiat. Res. 147:457-67
67. Packer AI, Besmer P, Bachvarova RF. 1995. Kit ligand mediates survival of type A spermatogonia and dividing spermatocytes in postnatal mouse testes. Mol. Reprod. Dev. 42:303-10
68. Richburg JH, Boekelheide K. 1996. Mono-(2-ethylhexyl) phthalate rapidly alters both Sertoli cell vimentin filaments and germ cell apoptosis in young rat testes. Toxicol. Appl. Pharmacol. 137:42-50
69. Yin Y, Hawkins KL, DeWolf WC, Morgentaler A. 1997. Heat stress causes testicular germ cell apoptosis in adult mice. J. Androl. 18:159-65
70. Koji T, Hishikawa Y, Ando H, Nakanishi Y, Kobayashi N. 2001. Expression of Fas and Fas ligand in normal and ischemia-reperfusion testes: involvement of the Fas system in the induction of germ cell apoptosis in the damaged mouse testis. Biol. Reprod. 64:946-54
71. Lee J, Richburg JH, Younkin SC, Boekelheide K. 1997. The Fas system is a key regulator of germ cell apoptosis in the testis. Endocrinology 138:2081-88
72. Wang R-A, Nakane PK, Koji T. 1998. Autonomous cell death of mouse male germ cells during fetal and postnatal period. Biol. Reprod. 58:1250-56
73. Xu JP, Li X, Mori E, Guo MW, Matsuda I, et al. 1999. Expression of Fas-Fas ligand in murine testis. Am. J. Reprod. Immunol. 42:381-88
74. Beumer TL, Roepers-Gajadien HL, Gademan IS, Lock TM, Kal HB, De Rooij DG. 2002. Apoptosis regulation in the testis: involvement of Bcl-2 family members. Mol. Reprod. Dev. 56:353-59
75. Embree-Ku M, Venturini D, Boekelheide K. 2002. Fas is involved in the p53-dependent apoptotic response to ionizing radiation in mouse testis. Biol. Reprod. 66:1456-61
76. Cryns V, Yuan J. 1998. Proteases to die for. Genes Dev. 12:1551-70
77. Hengartner MO. 1996. Programmed cell death in invertebrates. Curr. Opin. Genet. Dev. 6:34-38
78. Porter AG, Ng P, Janicke RU. 1997. Death substrates come alive. Bioessays 19: 501-7
79. Blanchard KT, Allard EK, Boekelheide K. 1996. Fate of germ cells in 2,5-hexanedione-induced testicular injury. I. Apoptosis is the mechanism of germ cell death. Toxicol. Appl. Pharmacol. 137:141-48
80. Lee J, Richburg JH, Shipp EB, Meistrich ML, Boekelheide K. 1999. The Fas system, a regulator of testicular germ cell apoptosis, is differentially upregulated in Sertoli cell versus germ cell injury of the testis. Endocrinology 140:852-58
81. Richburg JH, Nañez A, Williams LR, Embree ME, Boekelheide K. 2000. Sensitivity of testicular germ cells to toxicant-induced apoptosis in gld mice that express a non-functional form of FasL. Endocrinology 141:787-93
82. Mauduit C, Hamamah S, Benahmed M. 1999. Stem cell factor/c-kit system in spermatogenesis. Hum. Reprod. Update 5:535-45
83. Qiu FH, Ray P, Brown K, Barker PE, Jhanwar S, et al. 1988. Primary structure of c-kit: relationship with the CSF-1/PDGF receptor kinase family-oncogenic activation of v-kit involves deletion of extracellular domain and C terminus. EMBO J. 7:1003-11
84. Yarden Y, Kuang WJ, Yang-Feng T, Coussens L, Munemitsu S, et al. 1987. Human proto-oncogene c-kit: a new cell surface receptor tyrosine kinase for an unidentified ligand. EMBO J. 6:3341-51
85. Morrison-Graham K, Takahashi Y. 1993. Steel factor and c-kit receptor: from mutants to a growth factor system. Bioessays 15:77-83
86. Rossi P, Sette C, Dolci S, Geremia R. 2000. Role of c-kit in mammalian spermatogenesis. J. Endocrinol. Invest. 23:609-15
87. Sette C, Dolci S, Geremia R, Rossi P. 2000. The role of stem cell factor and of alternative c-kit gene products in the establishment, maintenance and function of germ cells. Int. J. Dev. Biol. 44:599-608
88. Ogawa T, Dobrinski I, Avarbock MR, Brinster RL. 2000. Transplantation of male germ line stem cells restores fertility in infertile mice. Nat. Med. 6:29-34
89. Kanatsu-Shinohara M, Ogura A, Ikegawa M, Inoue K, Ogonuki N, et al. 2002. Adenovirus-mediated gene delivery and in vitro microinsemination produce offspring from infertile male mice. Proc. Natl. Acad. Sci. USA 99:1383-88
90. Yoshinaga K, Nishikawa S, Ogawa M, Hayashi S, Kunisada T, et al. 1991. Role of c-kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c-kit expression and function. Development 113:689-99
91. Allard EK, Blanchard KT, Boekelheide K. 1996. Exogenous stem cell factor (SCF) compensates for altered endogenous SCF expression in 2,5-hexanedione-induced testicular atrophy in rats. Biol. Reprod. 55:185-93
92. Allard EK, Hall SJ, Boekelheide K. 1995. Stem cell kinetics in rat testis after irreversible injury induced by 2,5-hexanedione. Biol. Reprod. 53:186-92
93. Blanchard KT, Lee J, Boekelheide K. 1998. Leuprolide, a gonadotropin-releasing hormone agonist, reestablishes spermatogenesis after 2,5-hexanedione-induced irreversible testicular injury in the rat, resulting in normalized stem cell factor expression. Endocrinology 139:236-44
94. Brannan CI, Bedell MA, Resnick JL, Eppig JJ, Handel MA, et al. 1992. Developmental abnormalities in Steel17H mice result from a splicing defect in the steel factor cytoplasmic tail. Genes Dev. 6: 1832-42
95. Tajima Y, Onoue H, Kitamura Y, Nishimune Y. 1991. Biologically active kit ligand growth factor is produced by mouse Sertoli cells and is defective in SId mutant mice. Development 113:1031-35
96. Marziali G, Lazzaro D, Sorrentino V. 1993. Binding of germ cells to mutant SId Sertoli cells is defective and is rescued by expression of the transmembrane form of the c-kit ligand. Dev. Biol. 157:182-90
97. Jordan SA, Speed RM, Jackson IJ. 1999. Deficiency of Trp53 rescues the male fertility defects of Kit(W-v) mice but has no effect on the survival of melanocytes and mast cells. Dev. Biol. 215:78-90
98. Yan W, Suominen J, Samson M, Jegou B, Toppari J. 2000. Involvement of Bcl-2 family proteins in germ cell apoptosis during testicular development in the rat and pro-survival effect of stem cell factor on germ cells in vitro. Mol. Cell Endocrinol. 165:115-29
99. Meistrich ML, Kangasniemi M. 1997. Hormone treatment after irradiation stimulates recovery of rat spermatogenesis from surviving spermatogonia. J. Androl. 18:80-87
100. Shuttlesworth GA, de Rooij DG, Huhtaniemi I, Reissman T, Russell LD, et al. 2000. Enhancement of a spermatogonial proliferation and differentiation in irradiated rats by gonadeotropin-releasing hormone antagonist administration. Endocrinology 141:37-49
101. Meistrich ML, Wilson G, Huhtaniemi I. 1999. Hormonal treatment after cytotoxic therapy stimulates recovery of spermatogenesis. Cancer Res. 59:3557-60
102. Meistrich ML, Wilson G, Kangasniemi M, Huhtaniemi I. 2000. Mechanism of protection of rat spermatogenesis by hormonal pretreatment: stimulation of spermatogonial differentiation after irradiation. J. Androl. 21:464-69
103. Shetty G, Wilson G, Huhtaniemi I, Shutflesworth GA, Reissman T, Meistrich M. 2000. Gonadotropin-releasing hormone analogs stimulate and testosterone inhibits the recovery of spermatogenesis in irradiated rats. Endocrinology 141:1735-45
104. Schoenfeld HA, Boekelheide K, Shetty G, Meistrich ML. 2002. Reversal of toxicant-induced testicular atrophy: models and mechanisms. Toxicol. Sci. 66(1-S): 174(Abstr.)
105. Vogl AW, Linck RW, Dym M. 1983. Colchicine-induced changes in the cytoskeleton of the golden-mantled ground squirrel (Spermophilus lateralis) Sertoli cells. Am. J. Anat. 168:99-108
106. Russell LD, Malone JP, MacCurdy DS. 1981. Effect of the microtubule disrupting agents, colchicine and vinblastine, on seminiferous tubule structure in the rat. Tissue Cell 13:349-67
107. Russell LD, Saxena NK, Tumer TT. 1989. Cytoskeletal involvement in spermiation and sperm transport. Tissue Cell 21:361-79
108. O'Gorman S, Dagenais NA, Qian M, Marchuk Y. 1997. Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells. Proc. Natl. Acad. Sci. USA 94:14602-7
109. Blanchard KT, Boekelheide K. 1997. Adenovirus-mediated gene transfer to rat testis in vivo. Biol. Reprod. 56:495-500
110. Yamamoto H, Ochiya T, Tamamushi S, Toriyama-Baba H, Takahama Y, et al. 2002. HST-1/FGF-4 gene activation induces spermatogenesis and prevents adriamycin-induced testicular toxicity. Oncogene 21:899-908
111. Scobey M, Bertera S, Somers J, Watkins S, Zeleznik A, Walker W. 2001. Delivery of a cyclic adenosine 3′,5′-monophosphate response element-binding protein (creb) mutant to seminiferous tubules results in impaired spermatogenesis. Endocrinology 142:948-54
112. Leask A, Stearns T. 1998. Expression of amino- and carboxyl-terminal gamma-and alpha-tubulin mutants in cultured epithelial cells. J. Biol. Chem. 273:2661-68
113. Shu HB, Joshi HC. 1995. Gamma-tubulin can both nucleate microtubule assembly and self-assemble into novel tubular structures in mammalian cells. J. Cell Biol. 130:1137-47
114. Horio T, Basaki A, Takeoka A, Yamato M. 1999. Lethal level overexpression of gamma-tubulin in fission yeast causes mitotic arrest. Cell Motil. Cytoskeleton 44: 284-95
115. Horio T, Oakley BR. 1994. Human gamma-tubulin functions in fission yeast. J. Cell Biol. 126:1465-73
116. Leguy R, Melki R, Pantaloni D, Carlier MF. 2000. Monomeric gamma-tubulin nucleates microtubules. J. Biol. Chem. 275:21975-80
117. Wiese C, Zheng Y. 2000. A new function for the gamma-tubulin ring complex as a microtubule minus-end cap. Nat. Cell Biol. 2:35864
118. Wiese C, Zheng Y. 1999. Gamma-tubulin complexes and their interaction with microtubule-organizing centers. Curr. Opin. Struct. Biol. 9:250-59
119. Vogl AW. 1988. Changes in the distribution of microtubules in rat Sertoli cells during spermatogenesis. Anat. Rec. 222:34-41