Tubulin tyrosine ligase-like 1 deficiency results in chronic rhinosinusitis and abnormal development of spermatid flagella in mice

Veterinary Pathology

Volumn 47, Issue 4, 2010, Pages 703-712

  Vogel, Peter ^a   Hansen, G ^a   Fontenot, G ^a   Read, R ^a  

^a LEXICON PHARMACEUTICALS INC   (United States)

Author keywords

Flagella; Knockout mouse; Polyglutamylation; Primary ciliary dyskinesia; Spermatogenic arrest; Tubulin

Indexed keywords

PEPTIDE SYNTHASE; TUBULIN POLYGLUTAMYLASE;

ANIMAL; ARTICLE; C57BL MOUSE; CILIARY DYSKINESIA; CYTOCHEMISTRY; ENZYMOLOGY; FEMALE; FLAGELLUM; GENETICS; MALE; MALE INFERTILITY; MOUSE; MOUSE MUTANT; PATHOPHYSIOLOGY; PHYSIOLOGY; SPERMATID; KNOCKOUT MOUSE;

ANIMALS; CILIARY MOTILITY DISORDERS; FEMALE; FLAGELLA; HISTOCYTOCHEMISTRY; INFERTILITY, MALE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PEPTIDE SYNTHASES; SPERMATIDS;

MAMMALIA; MUS;

EID: 77954916671     PISSN: 03009858     EISSN: 15442217     Source Type: Journal    
DOI: 10.1177/0300985810363485     Document Type: Article

References (66)

1. Abuin A., Hansen GM, Zambrowicz B.: Gene trap mutagenesis. Handb Exp Pharmacol 178:129-147, 2007.
2. Afzelius BA: Cilia-related diseases. J Pathol 204:470-477, 2004.
3. Afzelius BA: A human syndrome caused by immotile cilia. Science 193:317-319, 1976.
4. Afzelius BA, Camner P., Mossberg B.: On the function of cilia in the female reproductive tract. Fertil Steril 29:72-74, 1978.
5. BeltrandelRio H., Kern F., Lanthorn T., Oravecz T., Piggott J., Powell D., Ramirez-Solis R., Sands AT, Zambrowicz BP: Saturation screening of the druggable mammalian genome. In: Model organisms in drug discovery, ed. Carroll PM and Fitzgerald K, pp. 251-279. John Wiley & Sons, Chichester, UK, 2003.
6. Bush A., Chodhari R., Collins N., Copeland F., Hall P., Harcourt J., Hariri M., Hogg C., Lucas J., Mitchison HM, O'Callaghan C., Phillips G.: Primary ciliary dyskinesia: current state of the art. Arch Dis Child 92:1136-1140, 2007.
7. Campbell PK, Waymire KG, Heier RL, Sharer C., Day DE, Reimann H., Jaje JM, Friedrich GA, Burmeister M., Bartness TJ, Russell LD, Young LJ, Zimmer M., Jenne DE, MacGregor GR: Mutation of a novel gene results in abnormal development of spermatid flagella, loss of intermale aggression and reduced body fat in mice. Genetics 162:307-320, 2002.
8. Carson JL, Collier AM: Ciliary defects: cell biology and clinical perspectives. Adv Pediatr 35:139-165, 1988.
9. Chilvers MA, McKean M., Rutman A., Myint BS, Silverman M., O'Callaghan C.: The effects of coronavirus on human nasal ciliated respiratory epithelium. Eur Respir J 18:965-970, 2001.
10. Davy BE, Robinson ML: Congenital hydrocephalus in hy3 mice is caused by a frameshift mutation in Hydin, a large novel gene. Hum Mol Genet 12:1163-1170, 2003.
11. Dutcher SK: Flagellar assembly in two hundred and fifty easy-to-follow steps. Trends Genet 11:398-404, 1995.
12. Edde B., Rossier J., Le Caer JP, Desbruyeres E., Gros F., Denoulet P.: Posttranslational glutamylation of alpha-tubulin. Science 247:83-85, 1990.
13. Edwards DF, Kennedy JR, Patton CS, Toal RL, Daniel GB, Lothrop CD: Familial immotile-cilia syndrome in English springer spaniel dogs. Am J Med Genet 33:290-298, 1989.
14. Edwards DF, Patton CS, Kennedy JR: Primary ciliary dyskinesia in the dog. Probl Vet Med 4:291-319, 1992.
15. Ersfeld K., Wehland J., Plessmann U., Dodemont H., Gerke V., Weber K.: Characterization of the tubulin-tyrosine ligase. J Cell Biol 120:725-732, 1993.
16. Escalier D.: Knockout mouse models of sperm flagellum anomalies. Hum Reprod Update 12:449-461, 2006.
17. Fernandez-Gonzalez A., Kourembanas S., Wyatt TA, Mitsialis SA: Mutation of murine adenylate kinase 7 underlies a primary ciliary dyskinesia phenotype. Am J Respir Cell Mol Biol 40:305-313, 2009.
18. Fliegauf M., Benzing T., Omran H.: When cilia go bad: cilia defects and ciliopathies. Nat Rev Mol Cell Biol 8:880-893, 2007.
19. Gagnon C., White D., Cosson J., Huitorel P., Edde B., Desbruyeres E., Paturle-Lafanechere L., Multigner L., Job D., Cibert C.: The poly-glutamylated lateral chain of alpha-tubulin plays a key role in flagellar motility. J Cell Sci 109:1545-1553, 1996.
20. Geremek M., Witt M.: Primary ciliary dyskinesia: genes, candidate genes and chromosomal regions. J Appl Genet 45:347-361, 2004.
21. Hansen GM, Markesich DC, Burnett MB, Zhu Q., Dionne KM, Richter LJ, Finnell RH, Sands AT, Zambrowicz BP, Abuin A.: Large-scale gene trapping in C57BL/6N mouse embryonic stem cells. Genome Res 18:1670-1679, 2008.
22. Huitorel P., White D., Fouquet JP, Kann ML, Cosson J., Gagnon C.: Differential distribution of glutamylated tubulin isoforms along the sea urchin sperm axoneme. Mol Reprod Dev 62:139-148, 2002.
23. Ibanez-Tallon I., Gorokhova S., Heintz N.: Loss of function of axonemal dynein Mdnah5 causes primary ciliary dyskinesia and hydrocephalus. Hum Mol Genet 11:715-721, 2002.
24. Ibanez-Tallon I., Pagenstecher A., Fliegauf M., Olbrich H., Kispert A., Ketelsen UP, North A., Heintz N., Omran H.: Dysfunction of axonemal dynein heavy chain Mdnah5 inhibits ependymal flow and reveals a novel mechanism for hydrocephalus formation. Hum Mol Genet 13:2133-2141, 2004.
25. Ikegami K., Horigome D., Mukai M., Livnat I., MacGregor GR, Setou M.: TTLL10 is a protein polyglycylase that can modify nucleosome assembly protein 1. FEBS Lett 582:1129-1134, 2008.
26. Inglis PN, Boroevich KA, Leroux MR: Piecing together a ciliome. Trends Genet 22:491-500, 2006.
27. Janke C., Rogowski K., van Dijk J.: Polyglutamylation: a fine-regulator of protein function? "Protein Modifications: Beyond the Usual Suspects" review series. EMBO Rep 9:636-641, 2008.
28. Janke C., Rogowski K., Wloga D., Regnard C., Kajava AV, Strub JM, Temurak N., van Dijk J., Boucher D., van Dorsselaer A., Suryavanshi S., Gaertig J., Edde B.: Tubulin polyglutamylase enzymes are members of the TTL domain protein family. Science 308:1758-1762, 2005.
29. Kennedy MP, Omran H., Leigh MW, Dell S., Morgan L., Molina PL, Robinson BV, Minnix SL, Olbrich H., Severin T., Ahrens P., Lange L., Morillas HN, Noone PG, Zariwala MA, Knowles MR: Congenital heart disease and other heterotaxic defects in a large cohort of patients with primary ciliary dyskinesia. Circulation 115:2814-2821, 2007.
30. Lee L., Campagna DR, Pinkus JL, Mulhern H., Wyatt TA, Sisson JH, Pavlik JA, Pinkus GS, Fleming MD: Primary ciliary dyskinesia in mice lacking the novel ciliary protein Pcdp1. Mol Cell Biol 28:949-957, 2008.
31. Leigh MW, Pittman JE, Carson JL, Ferkol TW, Dell SD, Davis SD, Knowles MR, Zariwala MA: Clinical and genetic aspects of primary ciliary dyskinesia/Kartagener syndrome. Genet Med 11:473-487, 2009.
32. Mall MA: Role of cilia, mucus, and airway surface liquid in mucociliary dysfunction: lessons from mouse models. J Aerosol Med Pulm Drug Deliv 21:13-24, 2008.
33. Marshall WF: The cell biological basis of ciliary disease. J Cell Biol 180:17-21, 2008.
34. Meeks M., Bush A.: Primary ciliary dyskinesia (PCD). Pediatr Pulmonol 29:307-316, 2000.
35. Mitchell DR: Speculations on the evolution of 9+2 organelles and the role of central pair microtubules. Biol Cell 96:691-696, 2004.
36. National Research Council: Guide for the Care and Use of Laboratory Animals. National Academy Press, Washington DC, 1996.
37. Neesen J., Kirschner R., Ochs M., Schmiedl A., Habermann B., Mueller C., Holstein AF, Nuesslein T., Adham I., Engel W.: Disruption of an inner arm dynein heavy chain gene results in asthenozoospermia and reduced ciliary beat frequency. Hum Mol Genet 10:1117-1128, 2001.
38. Nonaka S., Tanaka Y., Okada Y., Takeda S., Harada A., Kanai Y., Kido M., Hirokawa N.: Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 95:829-837, 1998.
39. O'Callaghan C., Chetcuti P., Moya E.: High prevalence of primary ciliary dyskinesia in a British Asian population. Arch Dis Child 95:51-52, 2010.
40. Ostrowski LE, Yin W., Rogers TD, Busalacchi KB, Chua M., O'Neal WK, Grubb BR: Conditional deletion of Dnaic1 in a murine model of primary ciliary dyskinesia causes chronic rhinosinusitis [published online ahead of print August 12, 2009]. Am J Respir Cell Mol Biol.
41. Pathak N., Obara T., Mangos S., Liu Y., Drummond IA: The zebrafish fleer gene encodes an essential regulator of cilia tubulin polyglutamylation. Mol Biol Cell 18:4353-4364, 2007.
42. Pedersen M.: Ciliary activity and pollution. Lung 168(Suppl):368-376, 1990.
43. Purcell EM: The efficiency of propulsion by a rotating flagellum. Proc Natl Acad Sci U S A 94:11307-11311, 1997.
44. Redeker V., Melki R., Prome D., Le Caer JP, Rossier J.: Structure of tubulin C-terminal domain obtained by subtilisin treatment: the major alpha and beta tubulin isotypes from pig brain are glutamylated. FEBS Lett 313:185-192, 1992.
45. Regnard C., Desbruyeres E., Huet JC, Beauvallet C., Pernollet JC, Edde B.: Polyglutamylation of nucleosome assembly proteins. J Biol Chem 275:15969-15976, 2000.
46. Regnard C., Fesquet D., Janke C., Boucher D., Desbruyeres E., Koulakoff A., Insina C., Travo P., Edde B.: Characterisation of PGs1, a subunit of a protein complex co-purifying with tubulin polyglutamylase. J Cell Sci 116:4181-4190, 2003.
47. Roperto F., Brunetti A., Saviano L., Galati P.: Morphologic alterations in the cilia of a cat. Vet Pathol 33:460-462, 1996.
48. Roperto F., Galati P., Troncone A., Rossacco P., Campofreda M.: Primary ciliary dyskinesia in pigs. J Submicrosc Cytol Pathol 23:233-236, 1991.
49. Rudiger M., Plessman U., Kloppel KD, Wehland J., Weber K.: Class II tubulin, the major brain beta tubulin isotype is polyglutamylated on glutamic acid residue 435. FEBS Lett 308:101-105, 1992.
50. Sapiro R., Kostetskii I., Olds-Clarke P., Gerton GL, Radice GL, Strauss IJ: Male infertility, impaired sperm motility, and hydrocephalus in mice deficient in sperm-associated antigen 6. Mol Cell Biol 22:6298-6305, 2002.
51. Satir P., Christensen ST: Overview of structure and function of mammalian cilia. Annu Rev Physiol 69:377-400, 2007.
52. Sleigh MA, Blake JR, Liron N.: The propulsion of mucus by cilia. Am Rev Respir Dis 137:726-741, 1988.
53. Stannard W., Rutman A., Wallis C., O'Callaghan C.: Central micro-tubular agenesis causing primary ciliary dyskinesia. Am J Respir Crit Care Med 169:634-637, 2004.
54. Sui H., Downing KH: Molecular architecture of axonemal microtubule doublets revealed by cryo-electron tomography. Nature 442:475-478, 2006.
55. Tanaka H., Iguchi N., Toyama Y., Kitamura K., Takahashi T., Kaseda K., Maekawa M., Nishimune Y.: Mice deficient in the axonemal protein Tektin-t exhibit male infertility and immotile-cilium syndrome due to impaired inner arm dynein function. Mol Cell Biol 24:7958-7964, 2004.
56. Torikata C., Kijimoto C., Koto M.: Ultrastructure of respiratory cilia of WIC-Hyd male rats: an animal model for human immotile cilia syndrome. Am J Pathol 138:341-347, 1991.
57. van Dijk J., Rogowski K., Miro J., Lacroix B., Edde B., Janke C.: A targeted multienzyme mechanism for selective microtubule polyglutamylation. Mol Cell 26:437-448, 2007.
58. Vogel P., Read R., Hansen G., Freay L., Zambrowicz B., Sands A.: Situs inversus and related ciliopathies in Dpcd-/-, Pkd111-/- and Nme7-/- mice [published online ahead of print August 7, 2009]. Vet Pathol.
59. Watson PJ, Herrtage ME, Peacock MA, Sargan DR: Primary ciliary dyskinesia in Newfoundland dogs. Vet Rec 144:718-725, 1999.
60. Wloga D., Rogowski K., Sharma N., Van Dijk J., Janke C., Edde B., Bre MH, Levilliers N., Redeker V., Duan J., Gorovsky MA, Jerka-Dziadosz M., Gaertig J.: Glutamylation on alpha-tubulin is not essential but affects the assembly and functions of a subset of microtubules in Tetrahymena thermophila. Eukaryot Cell 7:1362-1372, 2008.
61. Yokoyama R., O'Toole E., Ghosh S., Mitchell DR: Regulation of flagellar dynein activity by a central pair kinesin. Proc Natl Acad Sci U S A 101:17398-17403, 2004.
62. Zambrowicz BP, Abuin A., Ramirez-Solis R., Richter LJ, Piggott J., BeltrandelRio H., Buxton EC, Edwards J., Finch RA, Friddle CJ, Gupta A., Hansen G., Hu Y., Huang W., Jaing C., Key BW, Jr., Kipp P., Kohlhauff B., Ma ZQ, Markesich D., Payne R., Potter DG, Qian N., Shaw J., Schrick J., Shi ZZ, Sparks MJ, Van Sligtenhorst I., Vogel P., Walke W., Xu N., Zhu Q., Person C., Sands AT: Wnk1 kinase deficiency lowers blood pressure in mice: a gene-trap screen to identify potential targets for therapeutic intervention. Proc Natl Acad Sci U S A 100:14109-14114, 2003.
63. Zambrowicz BP, Turner CA, Sands AT: Predicting drug efficacy: knockouts model pipeline drugs of the pharmaceutical industry. Curr Opin Pharmacol 3:563-570, 2003.
64. Zariwala M., O'Neal WK, Noone PG, Leigh MW, Knowles MR, Ostrowski LE: Investigation of the possible role of a novel gene, DPCD, in primary ciliary dyskinesia. Am J Respir Cell Mol Biol 30:428-434, 2004.
65. Zhang Z., Tang W., Zhou R., Shen X., Wei Z., Patel AM, Povlishock JT, Bennett J., Strauss JF 3rd: Accelerated mortality from hydrocephalus and pneumonia in mice with a combined deficiency of SPAG6 and SPAG16L reveals a functional interrelationship between the two central apparatus proteins. Cell Motil Cytoskeleton 64:360-376, 2007.
66. Zheng B., Sage M., Cai WW, Thompson DM, Tavsanli BC, Cheah YC, Bradley A.: Engineering a mouse balancer chromosome. Nat Genet 22:375-378, 1999.