Molecular characterization of Caveolin-1 in pigs infected with Haemophilus parasuis

Journal of Immunology

Volumn 186, Issue 5, 2011, Pages 3031-3046

  Liu, Xiang Dong ^a   Chen, Hong Bo ^a   Tong, Qin ^a   Li, Xin Yun ^a   Zhu, Meng Jin ^a   Wu, Zhen Fang ^b   Zhou, Rui ^a   Zhao, Shu Hong ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; CAVEOLIN 1 ALPHA; CAVEOLIN 1 BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; POLYCYTIDYLIC ACID; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BREEDING; CAV1 GENE; CONTROLLED STUDY; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENE MAPPING; GENE MUTATION; GENETIC ANALYSIS; GENETIC MARKER; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HAEMOPHILUS INFECTION; HAEMOPHILUS PARASUIS; IMMUNOLOGICAL PARAMETERS; KIDNEY CELL; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; SWINE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CATTLE; CAVEOLIN 1; CELL LINE; CHICKENS; DOWN-REGULATION; FEMALE; GENETIC VARIATION; HAEMOPHILUS INFECTIONS; HAEMOPHILUS PARASUIS; HUMANS; LIPOPOLYSACCHARIDES; MALE; MICE; MOLECULAR SEQUENCE DATA; POLY I-C; PROTEIN ISOFORMS; RATS; RNA, MESSENGER; SPECIES SPECIFICITY; SWINE; SWINE DISEASES; ZEBRAFISH;

EID: 79952757471     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902687     Document Type: Article

References (79)

1. Palade, G. E. 1953. The fine structure of blood capillaries. J. Appl. Phys. 24: 1424.
2. Yamada, E. 1955. The fine structure of the gall bladder epithelium of the mouse. J. Biophys. Biochem. Cytol. 1: 445-458.
3. Rothberg, K. G., J. E. Heuser, W. C. Donzell, Y. S. Ying, J. R. Glenney, and R. G. Anderson. 1992. Caveolin, a protein component of caveolae membrane coats. Cell 68: 673-682.
4. Williams, T. M., and M. P. Lisanti. 2004. The caveolin proteins. Genome Biol. 5: 214.
5. Zhu, Z., Y. Li, D. Mo, K. Li, and S. Zhao. 2006. Molecular characterization and expression analysis of the porcine caveolin-3 gene. Biochem. Biophys. Res. Commun. 346: 7-13.
6. Razani, B., S. E. Woodman, and M. P. Lisanti. 2002. Caveolae: from cell biology to animal physiology. Pharmacol. Rev. 54: 431-467.
7. Parton, R. G., and K. Simons. 2007. The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. 8: 185-194.
8. Harris, J., D. Werling, J. C. Hope, G. Taylor, and C. J. Howard. 2002. Caveolae and caveolin in immune cells: distribution and functions. Trends Immunol. 23: 158-164.
9. Juhász, M., M. Vértesaljai, L. Herszényi, P. Malfertheiner, M. P. Ebert, and Z. Tulassay. 2004. [The role of caveolin-1 gene in carcinogenesis]. Orv. Hetil. 145: 1985-1989.
10. Williams, T. M., and M. P. Lisanti. 2005. Caveolin-1 in oncogenic transformation, cancer, and metastasis. Am. J. Physiol. Cell Physiol. 288: C494-C506.
11. Shatz, M., and M. Liscovitch. 2004. Caveolin-1 and cancer multidrug resistance: coordinate regulation of pro-survival proteins? Leuk. Res. 28: 907-908. (Pubitemid 38953644)
12. Bouras, T., M. P. Lisanti, and R. G. Pestell. 2004. Caveolin-1 in breast cancer. Cancer Biol. Ther. 3: 931-941.
13. Medina, F. A., C. J. de Almeida, E. Dew, J. Li, G. Bonuccelli, T. M. Williams, A. W. Cohen, R. G. Pestell, P. G. Frank, H. B. Tanowitz, and M. P. Lisanti. 2006. Caveolin-1-deficient mice show defects in innate immunity and inflammatory immune response during Salmonella enterica serovar Typhimurium infection. Infect. Immun. 74: 6665-6674.
14. Li, J., A. Scherl, F. Medina, P. G. Frank, R. N. Kitsis, H. B. Tanowitz, F. Sotgia, and M. P. Lisanti. 2005. Impaired phagocytosis in caveolin-1 deficient macrophages. Cell Cycle 4: 1599-1607.
15. Hu, G., R. D. Ye, M. C. Dinauer, A. B. Malik, and R. D. Minshall. 2008. Neutrophil caveolin-1 expression contributes to mechanism of lung inflammation and injury. Am. J. Physiol. Lung Cell. Mol. Physiol. 294: L178-L186.
16. Zemans, R., and G. P. Downey. 2008. Role of caveolin-1 in regulation of inflammation: different strokes for different folks. Am. J. Physiol. Lung Cell. Mol. Physiol. 294: L175-L177.
17. Shin, J. S., and S. N. Abraham. 2001. Cell biology. Caveolae-not just craters in the cellular landscape. Science 293: 1447-1448.
18. Shin, J.-S., and S. N. Abraham. 2001. Caveolae as portals of entry for microbes. Microbes Infect. 3: 755-761.
19. Baumler, A. J., B. M. Hargis, and R. M. Tsolis. 2000. Tracing the origins of Salmonella outbreaks. Science 287: 50-52.
20. Yue, M., F. Yang, J. Yang, W. Bei, X. Cai, L. Chen, J. Dong, R. Zhou, M. Jin, Q. Jin, and H. Chen. 2009. Complete genome sequence of Haemophilus parasuis SH0165. J. Bacteriol. 191: 1359-1360.
21. Lewis, C. R., M. Torremorell, L. Galina-Pantoja, and S. C. Bishop. 2009. Genetic parameters for performance traits in commercial sows estimated before and after an outbreak of porcine reproductive and respiratory syndrome. J. Anim. Sci. 87: 876-884.
22. Segalés, J., G. M. Allan, and M. Domingo. 2005. Porcine circovirus diseases. Anim. Health Res. Rev. 6: 119-142.
23. Greiser-Wilke, I., and V. Moennig. 2004. Vaccination against classical swine fever virus: limitations and new strategies. Anim. Health Res. Rev. 5: 223-226.
24. Pomeranz, L. E., A. E. Reynolds, and C. J. Hengartner. 2005. Molecular biology of pseudorabies virus: impact on neurovirology and veterinary medicine. Microbiol. Mol. Biol. Rev. 69: 462-500.
25. Wang, C., Y. Mei, L. Li, D. Mo, J. Li, H. Zhang, X. Tian, and Y. Chen. 2008. Molecular characterization and expression analysis of caveolin-1 in pig tissues. Sci. China C Life Sci. 51: 655-661.
26. Blanco, I., A. Canals, G. Evans, M. A. Mellencamp, C. Cia, N. Deeb, L. Wang, and L. Galina-Pantoja. 2008. Differences in susceptibility to Haemophilus parasuis infection in pigs. Can J Veterinary Res 72: 228-235. (Pubitemid 351771827)
27. Oliveira, S., and C. Pijoan. 2004. Haemophilus parasuis: new trends on diagnosis, epidemiology and control. Vet. Microbiol. 99: 1-12.
28. Thomas, J. W., J. W. Touchman, R. W. Blakesley, G. G. Bouffard, S. M. Beckstrom-Sternberg, E. H. Margulies, M. Blanchette, A. C. Siepel, P. J. Thomas, J. C. McDowell, et al. 2003. Comparative analyses of multi-species sequences from targeted genomic regions. Nature 424: 788-793. (Pubitemid 37021709)
29. Feng, Z., Z. L. Tang, K. Li, B. Liu, M. Yu, and S. H. Zhao. 2007. Molecular characterization of the BTG2 and BTG3 genes in fetal muscle development of pigs. Gene 403: 170-177.
30. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599.
31. Kapustin, Y., A. Souvorov, T. Tatusova, and D. Lipman. 2008. Splign: algorithms for computing spliced alignments with identification of paralogs. Biol. Direct 3: 20.
32. Sandelin, A., W. W. Wasserman, and B. Lenhard. 2004. ConSite: web-based prediction of regulatory elements using cross-species comparison. Nucleic Acids Res. 32(Web Server issue): W249-W252. (Pubitemid 38997338)
33. Yerle, M., P. Pinton, A. Robic, A. Alfonso, Y. Palvadeau, C. Delcros, R. Hawken, L. Alexander, C. Beattie, L. Schook, et al. 1998. Construction of a whole-genome radiation hybrid panel for high-resolution gene mapping in pigs. Cytogenet. Cell Genet. 82: 182-188.
34. Milan, D., R. Hawken, C. Cabau, S. Leroux, C. Genet, Y. Lahbib, G. Tosser, A. Robic, F. Hatey, L. Alexander, et al. 2000. IMpRH server: an RH mapping server available on the Web. Bioinformatics 16: 558-559.
35. Rothschild, M. F., Z. L. Hu, and Z. Jiang. 2007. Advances in QTL mapping in pigs. Int. J. Biol. Sci. 3: 192-197.
36. Hu, Z. L., and J. M. Reecy. 2007. Animal QTLdb: beyond a repository. A public platform for QTL comparisons and integration with diverse types of structural genomic information. Mamm. Genome 18: 1-4.
37. Hu, Z. L., S. Dracheva, W. Jang, D. Maglott, J. Bastiaansen, M. F. Rothschild, and J. M. Reecy. 2005. A QTL resource and comparison tool for pigs: PigQTLDB. Mamm. Genome 16: 792-800.
38. Zhang, W. S., X. Li, and J. B. Liu. 2007. Genetic variation of Bmy1 alleles in barley (Hordeum vulgare L.) investigated by CAPS analysis. Theor. Appl. Genet. 114: 1039-1050.
39. Nakamura, Y., T. Gojobori, and T. Ikemura. 2000. Codon usage tabulated from international DNA sequence databases: status for the year 2000. Nucleic Acids Res. 28: 292. (Pubitemid 30047783)
40. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
41. Kozak, M. 1986. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 44: 283-292. (Pubitemid 16048214)
42. Swimmer, C., and T. Shenk. 1985. Selection of sequence elements that substitute for the standard AATAAA motif which signals 3′ processing and polyadenylation of late simian virus 40 mRNAs. Nucleic Acids Res. 13: 8053-8063.
43. Wu, Q., and A. R. Krainer. 1996. U1-mediated exon definition interactions between AT-AC and GT-AG introns. Science 274: 1005-1008.
44. Long, M., C. Rosenberg, and W. Gilbert. 1995. Intron phase correlations and the evolution of the intron/exon structure of genes. Proc. Natl. Acad. Sci. USA 92: 12495-12499.
45. Hawken, R. J., J. Murtaugh, G. H. Flickinger, M. Yerle, A. Robic, D. Milan, J. Gellin, C. W. Beattie, L. B. Schook, and L. J. Alexander. 1999. A first-generation porcine whole-genome radiation hybrid map. Mamm. Genome 10: 824-830.
46. Engelman, J. A., X. L. Zhang, and M. P. Lisanti. 1998. Genes encoding human caveolin-1 and -2 are co-localized to the D7S522 locus (7q31.1), a known fragile site (FRA7G) that is frequently deleted in human cancers. FEBS Lett. 436: 403-410.
47. Goureau, A., M. Yerle, A. Schmitz, J. Riquet, D. Milan, P. Pinton, G. Frelat, and J. Gellin. 1996. Human and porcine correspondence of chromosome segments using bidirectional chromosome painting. Genomics 36: 252-262. (Pubitemid 26307487)
48. Edwards, D. B., C. W. Ernst, N. E. Raney, M. E. Doumit, M. D. Hoge, and R. O. Bates. 2008. Quantitative trait locus mapping in an F2 Duroc x Pietrain resource population: II. Carcass and meat quality traits. J. Anim. Sci. 86: 254-266.
49. Glenney, J. R., Jr. 1992. The sequence of human caveolin reveals identity with VIP21, a component of transport vesicles. FEBS Lett. 314: 45-48.
50. Glenney, J. R., Jr., and D. Soppet. 1992. Sequence and expression of caveolin, a protein component of caveolae plasma membrane domains phosphorylated on tyrosine in Rous sarcoma virus-transformed fibroblasts. Proc. Natl. Acad. Sci. USA 89: 10517-10521.
51. Engelman, J. A., X. L. Zhang, and M. P. Lisanti. 1999. Sequence and detailed organization of the human caveolin-1 and -2 genes located near the D7S522 locus (7q31.1). Methylation of a CpG island in the 59 promoter region of the caveolin-1 gene in human breast cancer cell lines. FEBS Lett. 448: 221-230.
52. Fra, A. M., E. Pasqualetto, M. Mancini, and R. Sitia. 2000. Genomic organization and transcriptional analysis of the human genes coding for caveolin-1 and caveolin-2. Gene 243: 75-83. (Pubitemid 30079707)
53. Kogo, H., and T. Fujimoto. 2000. Caveolin-1 isoforms are encoded by distinct mRNAs. Identification Of mouse caveolin-1 mRNA variants caused by alternative transcription initiation and splicing. FEBS Lett. 465: 119-123.
54. Razani, B., D. S. Park, Y. Miyanaga, A. Ghatpande, J. Cohen, X. B. Wang, P. E. Scherer, T. Evans, and M. P. Lisanti. 2002. Molecular cloning and developmental expression of the caveolin gene family in the amphibian Xenopus laevis. Biochemistry 41: 7914-7924.
55. Fang, P. K., K. R. Solomon, L. Zhuang, M. Qi, M. McKee, M. R. Freeman, and P. C. Yelick. 2006. Caveolin-1alpha and -1beta perform nonredundant roles in early vertebrate development. Am. J. Pathol. 169: 2209-2222.
56. Tang, Z., T. Okamoto, P. Boontrakulpoontawee, T. Katada, A. J. Otsuka, and M. P. Lisanti. 1997. Identification, sequence, and expression of an invertebrate caveolin gene family from the nematode Caenorhabditis elegans. Implications for the molecular evolution of mammalian caveolin genes. J. Biol. Chem. 272: 2437-2445.
57. Scherer, P. E., Z. Tang, M. Chun, M. Sargiacomo, H. F. Lodish, and M. P. Lisanti. 1995. Caveolin isoforms differ in their N-terminal protein sequence and subcellular distribution. Identification and epitope mapping of an isoform-specific monoclonal antibody probe. J. Biol. Chem. 270: 16395-16401.
58. Hernandez, N. 1993. TBP, a universal eukaryotic transcription factor? Genes Dev. 7(7B): 1291-1308.
59. Smale, S. T. 1997. Transcription initiation from TATA-less promoters within eukaryotic protein-coding genes. Biochim. Biophys. Acta 1351: 73-88.
60. Kozak, M. 1987. An analysis of 59-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 15: 8125-8148.
61. Kozak, M. 1984. Point mutations close to the AUG initiator codon affect the efficiency of translation of rat preproinsulin in vivo. Nature 308: 241-246. (Pubitemid 14132027)
62. Medina, F. A., T. M. Williams, F. Sotgia, H. B. Tanowitz, and M. P. Lisanti. 2006. A novel role for caveolin-1 in B lymphocyte function and the development of thymus-independent immune responses. Cell Cycle 5: 1865-1871.
63. Chidlow, J. H., Jr., J. J. Greer, C. Anthoni, P. Bernatchez, C. Fernadez-Hernando, M. Bruce, M. Abdelbaqi, D. Shukla, D. N. Granger, W. C. Sessa, and C. G. Kevil. 2009. Endothelial caveolin-1 regulates pathologic angiogenesis in a mouse model of colitis. Gastroenterology 136: 575-584.e572.
64. Kimchi-Sarfaty, C., J. M. Oh, I. W. Kim, Z. E. Sauna, A. M. Calcagno, S. V. Ambudkar, and M. M. Gottesman. 2007. A "silent" polymorphism in the MDR1 gene changes substrate specificity. Science 315: 525-528.
65. van Golen, K. L. 2006. Is caveolin-1 a viable therapeutic target to reduce cancer metastasis? Expert Opin. Ther. Targets 10: 709-721.
66. Engelman, J. A., X. L. Zhang, B. Razani, R. G. Pestell, and M. P. Lisanti. 1999. p42/44 MAP kinase-dependent and -independent signaling pathways regulate caveolin-1 gene expression. Activation of Ras-MAP kinase and protein kinase a signaling cascades transcriptionally down-regulates caveolin-1 promoter activity. J. Biol. Chem. 274: 32333-32341.
67. Wang, X. M., H. P. Kim, R. Song, and A. M. Choi. 2006. Caveolin-1 confers antiinflammatory effects in murine macrophages via the MKK3/p38 MAPK pathway. Am. J. Respir. Cell Mol. Biol. 34: 434-442.
68. Lei, M. G., and D. C. Morrison. 2000. Differential expression of caveolin-1 in lipopolysaccharide-activated murine macrophages. Infect. Immun. 68: 5084-5089.
69. Tiruppathi, C., J. Shimizu, K. Miyawaki-Shimizu, S. M. Vogel, A. M. Bair, R. D. Minshall, D. Predescu, and A. B. Malik. 2008. Role of NF-kappaB-dependent caveolin-1 expression in the mechanism of increased endothelial permeability induced by lipopolysaccharide. J. Biol. Chem. 283: 4210-4218.
70. van den Heuvel, A. P., A. Schulze, and B. M. Burgering. 2005. Direct control of caveolin-1 expression by FOXO transcription factors. Biochem. J. 385: 795-802.
71. Garrean, S., X. P. Gao, V. Brovkovych, J. Shimizu, Y. Y. Zhao, S. M. Vogel, and A. B. Malik. 2006. Caveolin-1 regulates NF-kappaB activation and lung inflammatory response to sepsis induced by lipopolysaccharide. J. Immunol. 177: 4853-4860.
72. Del Galdo, F., M. P. Lisanti, and S. A. Jimenez. 2008. Caveolin-1, transforming growth factor-beta receptor internalization, and the pathogenesis of systemic sclerosis. Curr. Opin. Rheumatol. 20: 713-719.
73. Del Galdo, F., F. Sotgia, C. J. de Almeida, J. F. Jasmin, M. Musick, M. P. Lisanti, and S. A. Jiménez. 2008. Decreased expression of caveolin 1 in patients with systemic sclerosis: crucial role in the pathogenesis of tissue fibrosis. Arthritis Rheum. 58: 2854-2865.
74. Ge, S., and J. S. Pachter. 2004. Caveolin-1 knockdown by small interfering RNA suppresses responses to the chemokine monocyte chemoattractant protein-1 by human astrocytes. J. Biol. Chem. 279: 6688-6695.
75. Jasmin, J. F., S. Malhotra, M. Singh Dhallu, I. Mercier, D. M. Rosenbaum, and M. P. Lisanti. 2007. Caveolin-1 deficiency increases cerebral ischemic injury. Circ. Res. 100: 721-729.
76. Trushina, E., J. Du Charme, J. Parisi, and C. T. McMurray. 2006. Neurological abnormalities in caveolin-1 knock out mice. Behav. Brain Res. 172: 24-32.
77. Stear, M. J., S. C. Bishop, B. A. Mallard, and H. Raadsma. 2001. The sustainability, feasibility and desirability of breeding livestock for disease resistance. Res. Vet. Sci. 71: 1-7.
78. Clapperton, M., S. C. Bishop, and E. J. Glass. 2005. Innate immune traits differ between Meishan and Large White pigs. Vet. Immunol. Immunopathol. 104: 131-144.
79. Gogolin-Ewens, K. J., E. N. Meeusen, P. C. Scott, T. E. Adams, and M. R. Brandon. 1990. Genetic selection for disease resistance and traits of economic importance in animal production. Rev. - Off. Int. Epizoot. 9: 865-896.