Whole genome microarray of the major pelvic ganglion after cavernous nerve injury: New insights into molecular profile changes after nerve injury

BJU International

Volumn 109, Issue 10, 2012, Pages 1552-1564

  Calenda, Giulia ^a   Strong, Travis D ^b   Pavlovich, Christian P ^b   Schaeffer, Edward M ^b   Burnett, Arthur L ^b   Yu, Wayne ^b   Davies, Kelvin P ^a   Bivalacqua, Trinity J ^b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

erectile dysfunction; microarray; nerve regeneration; pathway analysis; prostate cancer; radical prostatectomy

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; NERVE GROWTH FACTOR;

A2M GENE; ARG1 GENE; ARTICLE; ATF3 GENE; C3 GENE; CAVERNOUS NERVE INJURY; EGR4 GENE; FN1 GENE; GAL GENE; GANGLION; GENE; GENE EXPRESSION; GJA1 GENE; GJC1 GENE; HUMAN; IGF1 GENE; MAJOR PELVIC GANGLION; MICROARRAY ANALYSIS; MOLECULAR DYNAMICS; NERVE INJURY; NEUROPROTECTION; PLAU GENE; PLAUR GENE; PRIORITY JOURNAL; SERPINE1 GENE; SERPINE2 GENE; SERPINF1 GENE; STEM CELL; SYNAPTIC TRANSMISSION; TISSUE REPAIR; WHOLE GENOME MICROARRAY;

ANIMALS; BIOLOGICAL MARKERS; DISEASE MODELS, ANIMAL; ERECTILE DYSFUNCTION; GANGLIA; HYPOGASTRIC PLEXUS; MALE; NERVE REGENERATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PENILE ERECTION; PENIS; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; RNA; TRAUMA, NERVOUS SYSTEM;

EID: 84860350962     PISSN: 14644096     EISSN: 1464410X     Source Type: Journal    
DOI: 10.1111/j.1464-410X.2011.10705.x     Document Type: Article

References (75)

1. Meuleman EJ, Mulders PF,. Erectile function after radical prostatectomy: a review. Eur Urol 2003; 43: 95-101
2. Mulhall JP,. Penile rehabilitation following radical prostatectomy. Curr Opin Urol 2008; 18: 613-20
3. Ahlering TE, Rodriguez E, Skarecky DW,. Overcoming obstacles: nerve-sparing issues in radical prostatectomy. J Endourol 2008; 22: 745-50
4. Khatlani K, Sharma S, Mendoza PJ, Lee DI,. The current state of robot assisted radical prostatectomy. Minerva Urol Nefrol 2010; 62: 193-201
5. Correa JJ, Pow-Sang JM,. Optimizing cancer control and functional outcomes following robotic prostatectomy. Cancer Control 2010; 17: 233-44
6. Walsh PC,. The discovery of the cavernous nerves and development of nerve sparing radical retropubic prostatectomy. J Urol 2007; 177: 1632-5
7. Burnett AL, Aus G, Canby-Hagino ED, et al,. Erectile function outcome reporting after clinically localized prostate cancer treatment. J Urol 2007; 178: 597-601
8. Srivastava A, Tan G, Grover S, Tewari AK,. Nerve-sparing radical prostatectomy: current concepts in a robotic era. Panminerva Med 2010; 52: 223-30
9. Gallina A, Briganti A, Suardi N, et al,. Surgery and erectile dysfunction. Arch Esp Urol 2010; 63: 640-8
10. Hipp JD, Davies KP, Tar M, et al,. Using gene chips to identify organ-specific, smooth muscle responses to experimental diabetes: potential applications to urological diseases. BJU Int 2007; 99: 418-30
11. Kanika N, Chang J, Tong Y, et al,. Oxidative stress status accompanying diabetic bladder cystopathy results in the activation of protein degradation pathways. BJU Int 2011; 107: 1676-84
12. User HM, Zelner DJ, McKenna KE, McVary KT,. Microarray analysis and description of SMR1 gene in rat penis in a post-radical prostatectomy model of erectile dysfunction. J Urol 2003; 170: 298-301
13. Canguven O, Burnett A,. Cavernous nerve injury using rodent animal models. J Sex Med 2008; 5: 1776-85
14. Gratzke C, Strong TD, Gebska MA, et al,. Activated RhoA/Rho kinase impairs erectile function after cavernous nerve injury in rats. J Urol 2010; 184: 2197-204
15. Valentine H, Chen Y, Guo H, et al,. Neuroimmunophilin ligands protect cavernous nerves after crush injury in the rat: new experimental paradigms. Eur Urol 2007; 51: 1724-31
16. Bivalacqua TJ, Diner EK, Novak TE, et al,. A rat model of Peyronie's disease associated with a decrease in erectile activity and an increase in inducible nitric oxide synthase protein expression. J Urol 2000; 163: 1992-8
17. Dickinson TK, Connor JR,. Histological analysis of selected brain regions of hypotransferrinemic mice. Brain Res 1994; 635: 169-78
18. Ihaka RGR,. R: a language for data analysis and graphics. J Comput Graph Stat 1996; 5: 299-314
19. Zahurak M, Parmigiani G, Yu W, et al,. Pre-processing Agilent microarray data. BMC Bioinformatics 2007; 8: 142
20. Schaeffer EM, Marchionni L, Huang Z, et al,. Androgen-induced programs for prostate epithelial growth and invasion arise in embryogenesis and are reactivated in cancer. Oncogene 2008; 27: 7180-91
21. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I,. Controlling the false discovery rate in behavior genetics research. Behav Brain Res 2001; 125: 279-84
22. Calenda G, Tong Y, Tar M, et al,. Vcsa1 acts as a marker of erectile function recovery after gene therapeutic and pharmacological interventions. J Urol 2009; 181: 2806-15
23. Calenda G, Suadicani SO, Iglesias R, Spray DC, Melman A, Davies KP,. Silencing MaxiK activity in corporal smooth muscle cells initiates compensatory mechanisms to maintain calcium homeostasis. J Sex Med 2011; 8: 2191-204
24. Reichardt LF,. Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 2006; 361: 1545-64
25. Lin G, Shindel AW, Fandel TM, Bella AJ, Lin CS, Lue TF,. Neurotrophic effects of brain-derived neurotrophic factor and vascular endothelial growth factor in major pelvic ganglia of young and aged rats. BJU Int 2010; 105: 114-20
26. Bella AJ, Lin G, Tantiwongse K, et al,. Brain-derived neurotrophic factor (BDNF) acts primarily via the JAK/STAT pathway to promote neurite growth in the major pelvic ganglion of the rat: part I. J Sex Med 2006; 3: 815-20
27. Lin G, Bella AJ, Lue TF, Lin CS,. Brain-derived neurotrophic factor (BDNF) acts primarily via the JAK/STAT pathway to promote neurite growth in the major pelvic ganglion of the rat: part 2. J Sex Med 2006; 3: 821-7
28. Kato R, Wolfe D, Coyle CH, et al,. Herpes simplex virus vector-mediated delivery of glial cell line-derived neurotrophic factor rescues erectile dysfunction following cavernous nerve injury. Gene Ther 2007; 14: 1344-52
29. Lin G, Chen KC, Hsieh PS, Yeh CH, Lue TF, Lin CS,. Neurotrophic effects of vascular endothelial growth factor and neurotrophins on cultured major pelvic ganglia. BJU Int 2003; 92: 631-5
30. Pestov DG, Lau LF,. Genetic selection of growth-inhibitory sequences in mammalian cells. Proc Natl Acad Sci USA 1994; 91: 12549-53
31. Ramana CV, Gil MP, Schreiber RD, Stark GR,. Stat1-dependent and -independent pathways in IFN-gamma-dependent signaling. Trends Immunol 2002; 23: 96-101
32. Herdegen T, Leah JD,. Inducible and constitutive transcription factors in the mammalian nervous system: control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res Brain Res Rev 1998; 28: 370-490
33. Bella AJ, Lin G, Cagiannos I, Lue TF,. Emerging neuromodulatory molecules for the treatment of neurogenic erectile dysfunction caused by cavernous nerve injury. Asian J Androl 2008; 10: 54-9
34. Hiltunen JO, Laurikainen A, Klinge E, Saarma M,. Neurotrophin-3 is a target-derived neurotrophic factor for penile erection-inducing neurons. Neuroscience 2005; 133: 51-8
35. Laurikainen A, Hiltunen JO, Thomas-Crusells J, et al,. Neurturin is a neurotrophic factor for penile parasympathetic neurons in adult rat. J Neurobiol 2000; 43: 198-205
36. Chao MV, Lee FS,. Neurotrophin survival signaling mechanisms. J Alzheimers Dis 2004; 6: S7-11
37. Vivoli E, Di Cesare Mannelli L, Salvicchi A, et al,. Acetyl-L-carnitine increases artemin level and prevents neurotrophic factor alterations during neuropathy. Neuroscience 2010; 167: 1168-74
38. Sun ZH, Lai YL, Li P, Zuo HC, Xie ZP,. GDNF augments survival and differentiation of TH-positive neurons in neural progenitor cells. Cell Biol Int 2004; 28: 323-5
39. Ramer MS, Priestley JV, McMahon SB,. Functional regeneration of sensory axons into the adult spinal cord. Nature 2000; 403: 312-6
40. Linnarsson S, Mikaels A, Baudet C, Ernfors P,. Activation by GDNF of a transcriptional program repressing neurite growth in dorsal root ganglia. Proc Natl Acad Sci USA 2001; 98: 14681-6
41. Bella AJ, Fandel TM, Tantiwongse K, et al,. Neurturin enhances the recovery of erectile function following bilateral cavernous nerve crush injury in the rat. J Brachial Plex Peripher Nerve Inj 2007; 2: 5
42. Sofroniew MV, Howe CL, Mobley WC,. Nerve growth factor signaling, neuroprotection, and neural repair. Annu Rev Neurosci 2001; 24: 1217-81
43. Tuttle JB, Mackey T, Steers WD,. NGF, bFGF and CNTF increase survival of major pelvic ganglion neurons cultured from the adult rat. Neurosci Lett 1994; 173: 94-8
44. Tuttle JB, Steers WD,. Nerve growth factor responsiveness of cultured major pelvic ganglion neurons from the adult rat. Brain Res 1992; 588: 29-40
45. Hill CE, Harrison BJ, Rau KK, et al,. Skin incision induces expression of axonal regeneration-related genes in adult rat spinal sensory neurons. J Pain 2010; 11: 1066-73
46. Iismaa TP, Shine J,. Galanin and galanin receptors. Results Probl Cell Differ 1999; 26: 257-91
47. Bivalacqua TJ, Champion HC, Purohit SK, et al,. Nitric oxide-mediated erectile effects of galantide but not galanin in vivo. Nitric Oxide 2000; 4: 94-102
48. Dong MM, Yi TH,. Stem cell and peripheral nerve injury and repair. Facial Plast Surg 2010; 26: 421-7
49. Kingham PJ, Mantovani C, Terenghi G,. Stem cell and neuron co-cultures for the study of nerve regeneration. Methods Mol Biol 2011; 695: 115-27
50. Matsuse D, Kitada M, Kohama M, et al,. Human umbilical cord-derived mesenchymal stromal cells differentiate into functional Schwann cells that sustain peripheral nerve regeneration. J Neuropathol Exp Neurol 2010; 69: 973-85
51. Shokeir AA, Harraz AM, El-Din AB,. Tissue engineering and stem cells: basic principles and applications in urology. Int J Urol 2010; 17: 964-73
52. Bivalacqua TJ, Deng W, Kendirci M, et al,. Mesenchymal stem cells alone or ex vivo gene modified with endothelial nitric oxide synthase reverse age-associated erectile dysfunction. Am J Physiol Heart Circ Physiol 2007; 292: H1278-90
53. Bochinski D, Lin GT, Nunes L, et al,. The effect of neural embryonic stem cell therapy in a rat model of cavernosal nerve injury. BJU Int 2004; 94: 904-9
54. Hoke A,. Mechanisms of disease: what factors limit the success of peripheral nerve regeneration in humans? Nat Clin Pract Neurol 2006; 2: 448-54
55. Mukherjee PK, Marcheselli VL, Barreiro S, Hu J, Bok D, Bazan NG,. Neurotrophins enhance retinal pigment epithelial cell survival through neuroprotectin D1 signaling. Proc Natl Acad Sci USA 2007; 104: 13152-7
56. Falk T, Zhang S, Sherman SJ,. Pigment epithelium derived factor (PEDF) is neuroprotective in two in vitro models of Parkinson's disease. Neurosci Lett 2009; 458: 49-52
57. Bilak MM, Corse AM, Bilak SR, Lehar M, Tombran-Tink J, Kuncl RW,. Pigment epithelium-derived factor (PEDF) protects motor neurons from chronic glutamate-mediated neurodegeneration. J Neuropathol Exp Neurol 1999; 58: 719-28
58. Namba T, Yabe T, Gonda Y, et al,. Pigment epithelium-derived factor up-regulation induced by memantine, an N-methyl-D-aspartate receptor antagonist, is involved in increased proliferation of hippocampal progenitor cells. Neuroscience 2010; 167: 372-83
59. Volpert KN, Tombran-Tink J, Barnstable C, Layer PG,. PEDF and GDNF are key regulators of photoreceptor development and retinal neurogenesis in reaggregates from chick embryonic retina. J Ocul Biol Dis Infor 2009; 2: 1-11
60. Croci L, Barili V, Chia D, et al,. Local insulin-like growth factor I expression is essential for Purkinje neuron survival at birth. Cell Death Differ 2011; 18: 48-59
61. Siconolfi LB, Seeds NW,. Induction of the plasminogen activator system accompanies peripheral nerve regeneration after sciatic nerve crush. J Neurosci 2001; 21: 4336-47
62. Cai D, Deng K, Mellado W, Lee J, Ratan RR, Filbin MT,. Arginase I and polyamines act downstream from cyclic AMP in overcoming inhibition of axonal growth MAG and myelin in vitro. Neuron 2002; 35: 711-9
63. Estevez AG, Sahawneh MA, Lange PS, Bae N, Egea M, Ratan RR,. Arginase 1 regulation of nitric oxide production is key to survival of trophic factor-deprived motor neurons. J Neurosci 2006; 26: 8512-6
64. Dawson VL, Dawson TM, London ED, Bredt DS, Snyder SH,. Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc Natl Acad Sci USA 1991; 88: 6368-71
65. Ma TC, Campana A, Lange PS, et al,. A large-scale chemical screen for regulators of the arginase 1 promoter identifies the soy isoflavone daidzeinas a clinically approved small molecule that can promote neuronal protection or regeneration via a cAMP-independent pathway. J Neurosci 2010; 30: 739-48
66. Saul KE, Koke JR, Garcia DM,. Activating transcription factor 3 (ATF3) expression in the neural retina and optic nerve of zebrafish during optic nerve regeneration. Comp Biochem Physiol A Mol Integr Physiol 2010; 155: 172-82
67. O'Donovan KJ, Tourtellotte WG, Millbrandt J, Baraban JM,. The EGR family of transcription-regulatory factors: progress at the interface of molecular and systems neuroscience. Trends Neurosci 1999; 22: 167-73
68. Naus CC, Ozog MA, Bechberger JF, Nakase T,. A neuroprotective role for gap junctions. Cell Commun Adhes 2001; 8: 325-8
69. Chandross KJ, Kessler JA, Cohen RI, et al,. Altered connexin expression after peripheral nerve injury. Mol Cell Neurosci 1996; 7: 501-18
70. Farahani R, Pina-Benabou MH, Kyrozis A, et al,. Alterations in metabolism and gap junction expression may determine the role of astrocytes as 'good samaritans' or executioners. Glia 2005; 50: 351-61
71. Asklund T, Appelskog IB, Ammerpohl O, et al,. Gap junction-mediated bystander effect in primary cultures of human malignant gliomas with recombinant expression of the HSVtk gene. Exp Cell Res 2003; 284: 185-95
72. Hygge-Blakeman K, Brumovsky P, Hao JX, et al,. Galanin over-expression decreases the development of neuropathic pain-like behaviors in mice after partial sciatic nerve injury. Brain Res 2004; 1025: 152-8
73. Gardner J, Ghorpade A,. Tissue inhibitor of metalloproteinase (TIMP)-1: the TIMPed balance of matrix metalloproteinases in the central nervous system. J Neurosci Res 2003; 74: 801-6
74. Shin TY, Ryu JK, Jin HR, et al,. Increased cavernous expression of transforming growth factor-beta1 and activation of the smad signaling pathway affects erectile dysfunction in men with spinal cord injury. J Sex Med 2011; 8: 1454-62
75. Jin HR, Chung YG, Kim WJ, et al,. A mouse model of cavernous nerve injury-induced erectile dysfunction: functional and morphological characterization of the corpus cavernosum. J Sex Med 2010; 7: 3351-64