CHRFAM7A, a human-specific and partially duplicated α7-nicotinic acetylcholine receptor gene with the potential to specify a human-specific inflammatory response to injury

Journal of Leukocyte Biology

Volumn 97, Issue 2, 2015, Pages 247-257

  Costantini, Todd W ^a   Dang, Xitong ^a   Coimbra, Raul ^a   Eliceiri, Brian P ^a   Baird, Andrew ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

CHRNA7; Dup 7nAChR; Neuroinflammation; SLURP1; Vagus nerve; 7nAChR

Indexed keywords

ANTIBODY; BUNGAROTOXIN RECEPTOR; MESSENGER RNA; OLIGONUCLEOTIDE; CHRNA7 PROTEIN, HUMAN;

BRAIN; CHRFAM7A GENE; GENE STRUCTURE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INFECTION; INFLAMMATION; INJURY; LEUKOCYTE; MENTAL DISEASE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; VAGUS NERVE; CHANNEL GATING; DRUG DESIGN; GENE DUPLICATION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; PATHOLOGY;

ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; DRUG DESIGN; GENE DUPLICATION; GENE EXPRESSION REGULATION; HUMANS; INFECTION; INFLAMMATION; ION CHANNEL GATING; LEUKOCYTES; RNA, MESSENGER;

EID: 84929158676     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.4RU0814-381R     Document Type: Review

References (110)

1. Andersson, U., Tracey, K. J. (2012) Neural reflexes in inflammation and immunity. J. Exp. Med. 209, 1057–1068.
2. Metz, C. N., Tracey, K. J. (2005) It takes nerve to dampen inflammation. Nat. Immunol. 6, 756–757.
3. Tracey, K. J. (2009) Reflex control of immunity. Nat. Rev. Immunol. 9, 418–428.
4. Wang, H., Yu, M., Ochani, M., Amella, C. A., Tanovic, M., Susarla, S., Li, J. H., Wang, H., Yang, H., Ulloa, L., Al-Abed, Y., Czura, C. J., Tracey, K. J. (2003) Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421, 384–388.
5. Gault, J., Robinson, M., Berger, R., Drebing, C., Logel, J., Hopkins, J., Moore, T., Jacobs, S., Meriwether, J., Choi, M. J., Kim, E. J., Walton, K., Buiting, K., Davis, A., Breese, C., Freedman, R., Leonard, S. (1998) Genomic organization and partial duplication of the human alpha7 neuronal nicotinic acetylcholine receptor gene (CHRNA7). Genomics 52, 173–185.
6. Tracey, K. J. (2002) The inflammatory reflex. Nature 420, 853–859.
7. Tracey, K. J. (2007) Physiology and immunology of the cholinergic antiinflammatory pathway. J. Clin. Invest. 117, 289–296.
8. Olofsson, P. S., Rosas-Ballina, M., Levine, Y. A., Tracey, K. J. (2012) Rethinking inflammation: neural circuits in the regulation of immunity. Immunol. Rev. 248, 188–204.
9. De Jonge, W. J., van der Zanden, E. P., The, F. O., Bijlsma, M. F., van Westerloo, D. J., Bennink, R. J., Berthoud, H. R., Uematsu, S., Akira, S., van den Wijngaard, R. M., Boeckxstaens, G. E. (2005) Stimulation of the vagus nerve attenuates macrophage activation by activating the Jak2- STAT3 signaling pathway. Nat. Immunol. 6, 844–851.
10. Yoshikawa, H., Kurokawa, M., Ozaki, N., Nara, K., Atou, K., Takada, E., Kamochi, H., Suzuki, N. (2006) Nicotine inhibits the production of proinflammatory mediators in human monocytes by suppression of IkappaB phosphorylation and nuclear factor-kappaB transcriptional activity through nicotinic acetylcholine receptor alpha 7. Clin. Exp. Immunol. 146, 116–123.
11. Kees, M. G., Pongratz, G., Kees, F., Schölmerich, J., Straub, R. H. (2003) Via beta-adrenoceptors, stimulation of extrasplenic sympathetic nerve fibers inhibits lipopolysaccharide-induced TNF secretion in perfused rat spleen. J. Neuroimmunol. 145, 77–85.
12. Brandon, K. W., Rand, M. J. (1961) Acetylcholine and the sympathetic innervation of the spleen. J. Physiol. 157, 18–32.
13. Leaders, F. E., Dayrit, C. (1965) The cholinergic component in the sympathetic innervation to the spleen. J. Pharmacol. Exp. Ther. 147, 145–152.
14. Bellinger, D. L., Felten, S. Y., Lorton, D., Felten, D. L. (1989) Origin of noradrenergic innervation of the spleen in rats. Brain Behav. Immun. 3, 291–311.
15. Bellinger, D. L., Lorton, D., Hamill, R. W., Felten, S. Y., Felten, D. L. (1993) Acetylcholinesterase staining and choline acetyltransferase activity in the young adult rat spleen: lack of evidence for cholinergic innervation. Brain Behav. Immun. 7, 191–204.
16. Berthoud, H. R., Powley, T. L. (1993) Characterization of vagal innervation to the rat celiac, suprarenal and mesenteric ganglia. J. Auton. Nerv. Syst. 42, 153–169.
17. Huston, J. M., Ochani, M., Rosas-Ballina, M., Liao, H., Ochani, K., Pavlov, V. A., Gallowitsch-Puerta, M., Ashok, M., Czura, C. J., Foxwell, B., Tracey, K. J., Ulloa, L. (2006) Splenectomy inactivates the cholinergic antiinflammatory pathway during lethal endotoxemia and polymicrobial sepsis. J. Exp. Med. 203, 1623–1628.
18. Rosas-Ballina, M., Ochani, M., Parrish, W. R., Ochani, K., Harris, Y. T., Huston, J. M., Chavan, S., Tracey, K. J. (2008) Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia. Proc. Natl. Acad. Sci. USA 105, 11008–11013.
19. Rosas-Ballina, M., Olofsson, P. S., Ochani, M., Valdés-Ferrer, S. I., Levine, Y. A., Reardon, C., Tusche, M. W., Pavlov, V. A., Andersson, U., Chavan, S., Mak, T. W., Tracey, K. J. (2011) Acetylcholinesynthesizing T cells relay neural signals in a vagus nerve circuit. Science 334, 98–101.
20. Costantini, T. W., Bansal, V., Krzyzaniak, M., Putnam, J. G., Peterson, C. Y., Loomis, W. H., Wolf, P., Baird, A., Eliceiri, B. P., Coimbra, R. (2010) Vagal nerve stimulation protects against burn-induced intestinal injury through activation of enteric glia cells. Am. J. Physiol. Gastrointest. Liver Physiol. 299, G1308–G1318.
21. Costantini, T. W., Bansal, V., Peterson, C. Y., Loomis, W. H., Putnam, J. G., Rankin, F., Wolf, P., Eliceiri, B. P., Baird, A., Coimbra, R. (2010) Efferent vagal nerve stimulation attenuates gut barrier injury after burn: modulation of intestinal occludin expression. J. Trauma 68, 1349–1354; discussion 1354–1346.
22. Costantini, T. W., Krzyzaniak, M., Cheadle, G. A., Putnam, J. G., Hageny, A. M., Lopez, N., Eliceiri, B. P., Bansal, V., Coimbra, R. (2012) Targeting a-7 nicotinic acetylcholine receptor in the enteric nervous system: a cholinergic agonist prevents gut barrier failure after severe burn injury. Am. J. Pathol. 181, 478–486.
23. Costantini, T. W., Loomis, W. H., Putnam, J. G., Drusinsky, D., Deree, J., Choi, S., Wolf, P., Baird, A., Eliceiri, B., Bansal, V., Coimbra, R. (2009) Burn-induced gut barrier injury is attenuated by phosphodiesterase inhibition: effects on tight junction structural proteins. Shock 31, 416–422.
24. Costantini, T. W., Putnam, J. G., Sawada, R., Baird, A., Loomis, W. H., Eliceiri, B. P., Bansal, V., Coimbra, R. (2009) Targeting the gut barrier: identification of a homing peptide sequence for delivery into the injured intestinal epithelial cell. Surgery 146, 206–212.
25. Matteoli, G., Gomez-Pinilla, P. J., Nemethova, A., Di Giovangiulio, M., Cailotto, C., van Bree, S. H., Michel, K., Tracey, K. J., Schemann, M., Boesmans, W., Vanden Berghe, P., Boeckxstaens, G. E. (2014) A distinct vagal anti-inflammatory pathway modulates intestinal muscularis resident macrophages independent of the spleen. Gut 63, 938–948.
26. Kawashima, K., Fujii, T., Moriwaki, Y., Misawa, H., Horiguchi, K. (2012) Reconciling neuronally and nonneuronally derived acetylcholine in the regulation of immune function. Ann. N. Y. Acad. Sci. 1261, 7–17.
27. Grando, S. A. (2008) Basic and clinical aspects of non-neuronal acetylcholine: biological and clinical significance of non-canonical ligands of epithelial nicotinic acetylcholine receptors. J. Pharmacol. Sci. 106, 174–179.
28. Papke, R. L. (2014) Merging old and new perspectives on nicotinic acetylcholine receptors. Biochem. Pharmacol. 89, 1–11.
29. Séguéla, P., Wadiche, J., Dineley-Miller, K., Dani, J. A., Patrick, J. W. (1993) Molecular cloning, functional properties, and distribution of rat brain alpha 7: a nicotinic cation channel highly permeable to calcium. J. Neurosci. 13, 596–604.
30. Williams, D. K., Peng, C., Kimbrell, M. R., Papke, R. L. (2012) Intrinsically low open probability of a7 nicotinic acetylcholine receptors can be overcome by positive allosteric modulation and serum factors leading to the generation of excitotoxic currents at physiological temperatures. Mol. Pharmacol. 82, 746–759.
31. Williams, D. K., Wang, J., Papke, R. L. (2011) Investigation of the molecular mechanism of the a7 nicotinic acetylcholine receptor positive allosteric modulator PNU-120596 provides evidence for two distinct desensitized states. Mol. Pharmacol. 80, 1013–1032.
32. Sharma, G., Vijayaraghavan, S. (2002) Nicotinic receptor signaling in nonexcitable cells. J. Neurobiol. 53, 524–534.
33. Wessler, I., Kirkpatrick, C. J. (2008) Acetylcholine beyond neurons: the non-neuronal cholinergic system in humans. Br. J. Pharmacol. 154, 1558–1571.
34. Arredondo, J., Chernyavsky, A. I., Jolkovsky, D. L., Pinkerton, K. E., Grando, S. A. (2006) Receptor-mediated tobacco toxicity: cooperation of the Ras/Raf-1/MEK1/ERK and JAK-2/STAT-3 pathways downstream of alpha7 nicotinic receptor in oral keratinocytes. FASEB J. 20, 2093–2101.
35. De Jonge, W. J., Ulloa, L. (2007) The alpha7 nicotinic acetylcholine receptor as a pharmacological target for inflammation. Br. J. Pharmacol. 151, 915–929.
36. Papke, R. L., Bencherif, M., Lippiello, P. (1996) An evaluation of neuronal nicotinic acetylcholine receptor activation by quaternary nitrogen compounds indicates that choline is selective for the alpha 7 subtype. Neurosci. Lett. 213, 201–204.
37. Papke, R. L., Porter Papke, J. K. (2002) Comparative pharmacology of rat and human alpha7 nAChR conducted with net charge analysis. Br. J. Pharmacol. 137, 49–61.
38. Orr-Urtreger, A., Göldner, F. M., Saeki, M., Lorenzo, I., Goldberg, L., De Biasi, M., Dani, J. A., Patrick, J. W., Beaudet, A. L. (1997) Mice deficient in the alpha7 neuronal nicotinic acetylcholine receptor lack alpha-bungarotoxin binding sites and hippocampal fast nicotinic currents. J. Neurosci. 17, 9165–9171.
39. Parrish, W. R., Rosas-Ballina, M., Gallowitsch-Puerta, M., Ochani, M., Ochani, K., Yang, L. H., Hudson, L., Lin, X., Patel, N., Johnson, S. M., Chavan, S., Goldstein, R. S., Czura, C. J., Miller, E. J., Al-Abed, Y., Tracey, K. J., Pavlov, V. A. (2008) Modulation of TNF release by choline requires alpha7 subunit nicotinic acetylcholine receptor-mediated signaling. Mol. Med. 14, 567–574.
40. Pavlov, V. A., Ochani, M., Yang, L. H., Gallowitsch-Puerta, M., Ochani, K., Lin, X., Levi, J., Parrish, W. R., Rosas-Ballina, M., Czura, C. J., Larosa, G. J., Miller, E. J., Tracey, K. J., Al-Abed, Y. (2007) Selective alpha7-nicotinic acetylcholine receptor agonist GTS-21 improves survival in murine endotoxemia and severe sepsis. Crit. Care Med. 35, 1139–1144.
41. Pavlov, V. A., Parrish, W. R., Rosas-Ballina, M., Ochani, M., Puerta, M., Ochani, K., Chavan, S., Al-Abed, Y., Tracey, K. J. (2009) Brain acetylcholinesterase activity controls systemic cytokine levels through the cholinergic anti-inflammatory pathway. Brain Behav. Immun. 23, 41–45.
42. Pavlov, V. A., Tracey, K. J. (2012) The vagus nerve and the inflammatory reflex—linking immunity and metabolism. Nat. Rev. Endocrinol. 8, 743–754.
43. Macklin, K. D., Maus, A. D., Pereira, E. F., Albuquerque, E. X., Conti- Fine, B. M. (1998) Human vascular endothelial cells express functional nicotinic acetylcholine receptors. J. Pharmacol. Exp. Ther. 287, 435–439.
44. Nastrucci, C., Russo, P. (2012) A7 nAChR in airway respiratory epithelial cells. Curr. Drug Targets 13, 666–670.
45. Pillai, S., Chellappan, S. (2012) A7 Nicotinic acetylcholine receptor subunit in angiogenesis and epithelial to mesenchymal transition. Curr. Drug Targets 13, 671–679.
46. Cardinale, A., Nastrucci, C., Cesario, A., Russo, P. (2012) Nicotine: specific role in angiogenesis, proliferation and apoptosis. Crit. Rev. Toxicol. 42, 68–89.
47. Kabbani, N., Nordman, J. C., Corgiat, B. A., Veltri, D. P., Shehu, A., Seymour, V. A., Adams, D. J. (2013) Are nicotinic acetylcholine receptors coupled to G proteins? BioEssays 35, 1025–1034.
48. Villiger, Y., Szanto, I., Jaconi, S., Blanchet, C., Buisson, B., Krause, K. H., Bertrand, D., Romand, J. A. (2002) Expression of an alpha7 duplicate nicotinic acetylcholine receptor-related protein in human leukocytes. J. Neuroimmunol. 126, 86–98.
49. Zody, M. C., Garber, M., Sharpe, T., Young, S. K., Rowen, L., O’Neill, K., Whittaker, C. A., Kamal, M., Chang, J. L., Cuomo, C. A., Dewar, K., FitzGerald, M. G., Kodira, C. D., Madan, A., Qin, S., Yang, X., Abbasi, N., Abouelleil, A., Arachchi, H. M., Baradarani, L., Birditt, B., Bloom, S., Bloom, T., Borowsky, M. L., Burke, J., Butler, J., Cook, A., DeArellano, K., DeCaprio, D., Dorris III L., Dors, M., Eichler, E. E., Engels, R., Fahey, J., Fleetwood, P., Friedman, C., Gearin, G., Hall, J. L., Hensley, G., Johnson, E., Jones, C., Kamat, A., Kaur, A., Locke, D. P., Madan, A., Munson, G., Jaffe, D. B., Lui, A., Macdonald, P., Mauceli, E., Naylor, J. W., Nesbitt, R., Nicol, R., O’Leary, S. B., Ratcliffe, A., Rounsley, S., She, X., Sneddon, K. M., Stewart, S., Sougnez, C., Stone, S. M., Topham, K., Vincent, D., Wang, S., Zimmer, A. R., Birren, B. W., Hood, L., Lander, E. S., Nusbaum, C. (2006) Analysis of the DNA sequence and duplication history of human chromosome 15. Nature 440, 671–675.
50. Le Novère, N., Corringer, P. J., Changeux, J. P. (2002) The diversity of subunit composition in nAChRs: evolutionary origins, physiologic and pharmacologic consequences. J. Neurobiol. 53, 447–456.
51. Locke, D. P., Archidiacono, N., Misceo, D., Cardone, M. F., Deschamps, S., Roe, B., Rocchi, M., Eichler, E. E. (2003) Refinement of a chimpanzee pericentric inversion breakpoint to a segmental duplication cluster. Genome Biol. 4, R50.
52. Riley, B., Williamson, M., Collier, D., Wilkie, H., Makoff, A. (2002) A 3- Mb map of a large segmental duplication overlapping the alpha7- nicotinic acetylcholine receptor gene (CHRNA7) at human 15q13-q 14. Genomics 79, 197–209.
53. Flomen, R. H., Davies, A. F., Di Forti, M., La Cascia, C., Mackie-Ogilvie, C., Murray, R., Makoff, A. J. (2008) The copy number variant involving part of the alpha7 nicotinic receptor gene contains a polymorphic inversion. Eur. J. Hum. Genet. 16, 1364–1371.
54. Freedman, R., Leonard, S., Gault, J. M., Hopkins, J., Cloninger, C. R., Kaufmann, C. A., Tsuang, M. T., Farone, S. V., Malaspina, D., Svrakic, D. M., Sanders, A., Gejman, P. (2001) Linkage disequilibrium for schizophrenia at the chromosome 15q13-14 locus of the alpha7- nicotinic acetylcholine receptor subunit gene (CHRNA7). Am. J. Med. Genet. 105, 20–22.
55. Freedman, R., Leonard, S., Waldo, M., Gault, J., Olincy, A., Adler, L. E. (2006) Characterization of allelic variants at chromosome 15q14 in schizophrenia. Genes Brain Behav. 5 (Suppl 1), 14–22.
56. Iwata, Y., Nakajima, M., Yamada, K., Nakamura, K., Sekine, Y., Tsuchiya, K. J., Sugihara, G., Matsuzaki, H., Suda, S., Suzuki, K., Takei, N., Mori, N., Iwayama, Y., Takao, H., Yoshikawa, T., Riley, B., Makoff, A., Sham, P., Chen, R., Collier, D. (2007) Linkage disequilibrium analysis of the CHRNA7 gene and its partially duplicated region in schizophrenia. Neurosci. Res. 57, 194–202.
57. Petrovsky, N., Schmechtig, A., Flomen, R. H., Kumari, V., Collier, D., Makoff, A., Wagner, M., Ettinger, U. (2009) CHRFAM7A copy number and 2-bp deletion polymorphisms and antisaccade performance. Int. J. Neuropsychopharmacol. 12, 267–273.
58. Sinkus, M. L., Lee, M. J., Gault, J., Logel, J., Short, M., Freedman, R., Christian, S. L., Lyon, J., Leonard, S. (2009) A 2-base pair deletion polymorphism in the partial duplication of the alpha7 nicotinic acetylcholine gene (CHRFAM7A) on chromosome 15q14 is associated with schizophrenia. Brain Res. 1291, 1–11.
59. De Luca, V., Likhodi, O., Van Tol, H. H., Kennedy, J. L., Wong, A. H. (2006) Regulation of alpha7-nicotinic receptor subunit and alpha7-like gene expression in the prefrontal cortex of patients with bipolar disorder and schizophrenia. Acta Psychiatr. Scand. 114, 211–215.
60. Flomen, R. H., Collier, D. A., Osborne, S., Munro, J., Breen, G., St Clair, D., Makoff, A. J. (2006) Association study of CHRFAM7A copy number and 2 bp deletion polymorphisms with schizophrenia and bipolar affective disorder. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 141B, 571–575.
61. Hong, C. J., Lai, I. C., Liou, L. L., Tsai, S. J. (2004) Association study of the human partially duplicated alpha7 nicotinic acetylcholine receptor genetic variant with bipolar disorder. Neurosci. Lett. 355, 69–72.
62. Dempster, E. L., Toulopoulou, T., McDonald, C., Bramon, E., Walshe, M., Wickham, H., Sham, P. C., Murray, R. M., Collier, D. A. (2006) Episodic memory performance predicted by the 2bp deletion in exon 6 of the “alpha 7-like” nicotinic receptor subunit gene. Am. J. Psychiatry 163, 1832–1834.
63. Fehér, A., Juhász, A., Rimanóczy, A., Csibri, E., Kálmán, J., Janka, Z. (2009) Association between a genetic variant of the alpha-7 nicotinic acetylcholine receptor subunit and four types of dementia. Dement. Geriatr. Cogn. Disord. 28, 56–62.
64. Swaminathan, S., Huentelman, M. J., Corneveaux, J. J., Myers, A. J., Faber, K. M., Foroud, T., Mayeux, R., Shen, L., Kim, S., Turk, M., Hardy, J., Reiman, E. M., Saykin, A. J.; Alzheimer’s Disease Neuroimaging Initiative and NIA-LOAD/NCRAD Family Study Group. (2012) Analysis of copy number variation in Alzheimer’s disease in a cohort of clinically characterized and neuropathologically verified individuals. PLoS One 7, e50640.
65. Swaminathan, S., Kim, S., Shen, L., Risacher, S. L., Foroud, T., Pankratz, N., Potkin, S. G., Huentelman, M. J., Craig, D. W., Weiner, M. W., Saykin, A. J.; The Alzheimer’s Disease Neuroimaging Initiative Adni. (2011) Genomic Copy Number Analysis in Alzheimer’s Disease and Mild Cognitive Impairment: An ADNI study. Int. J. Alzheimers Dis. 2011, 729478.
66. Swaminathan, S., Shen, L., Kim, S., Inlow, M., West, J. D., Faber, K. M., Foroud, T., Mayeux, R., Saykin, A. J.; Alzheimer’s Disease Neuroimaging Initiative; NIA-LOAD/NCRAD Family Study Group. (2012) Analysis of copy number variation in Alzheimer’s disease: the NIALOAD/NCRAD family study. Curr. Alzheimer Res. 9, 801–814.
67. Manchia, M., Viggiano, E., Tiwari, A. K., Renou, J., Jain, U., De Luca, V., Kennedy, J. L. (2010) Smoking in adult attention-deficit/hyperactivity disorder: interaction between 15q13 nicotinic genes and Temperament Character Inventory scores. World J. Biol. Psychiatry 11, 506–510.
68. Casey, J. P., Magalhaes, T., Conroy, J. M., Regan, R., Shah, N., Anney, R., Shields, D. C., Abrahams, B. S., Almeida, J., Bacchelli, E., Bailey, A. J., Baird, G., Battaglia, A., Berney, T., Bolshakova, N., Bolton, P. F., Bourgeron, T., Brennan, S., Cali, P., Correia, C., Corsello, C., Coutanche, M., Dawson, G., de Jonge, M., Delorme, R., Duketis, E., Duque, F., Estes, A., Farrar, P., Fernandez, B. A., Folstein, S. E., Foley, S., Fombonne, E., Freitag, C. M., Gilbert, J., Gillberg, C., Glessner, J. T., Green, J., Guter, S. J., Hakonarson, H., Holt, R., Hughes, G., Hus, V., Igliozzi, R., Kim, C., Klauck, S. M., Kolevzon, A., Lamb, J. A., Leboyer, M., Le Couteur, A., Leventhal, B. L., Lord, C., Lund, S. C., Maestrini, E., Mantoulan, C., Marshall, C. R., McConachie, H., McDougle, C. J., McGrath, J., McMahon, W. M., Merikangas, A., Miller, J., Minopoli, F., Mirza, G. K., Munson, J., Nelson, S. F., Nygren, G., Oliveira, G., Pagnamenta, A. T., Papanikolaou, K., Parr, J. R., Parrini, B., Pickles, A., Pinto, D., Piven, J., Posey, D. J., Poustka, A., Poustka, F., Ragoussis, J., Roge, B., Rutter, M. L., Sequeira, A. F., Soorya, L., Sousa, I., Sykes, N., Stoppioni, V., Tancredi, R., Tauber, M., Thompson, A. P., Thomson, S., Tsiantis, J., Van Engeland, H., Vincent, J. B., Volkmar, F., Vorstman, J. A., Wallace, S., Wang, K., Wassink, T. H., White, K., Wing, K., Wittemeyer, K., Yaspan, B. L., Zwaigenbaum, L., Betancur, C., Buxbaum, J. D., Cantor, R. M., Cook, E. H., Coon, H., Cuccaro, M. L., Geschwind, D. H., Haines, J. L., Hallmayer, J., Monaco, A. P., Nurnberger, Jr., J. I., Pericak-Vance, M. A., Schellenberg, G. D., Scherer, S. W., Sutcliffe, J. S., Szatmari, P., Vieland, V. J., Wijsman, E. M., Green, A., Gill, M., Gallagher, L., Vicente, A., Ennis, S. (2012) A novel approach of homozygous haplotype sharing identifies candidate genes in autism spectrum disorder. Hum. Genet. 131, 565–579.
69. Melchior, L., Bertelsen, B., Debes, N. M., Groth, C., Skov, L., Mikkelsen, J. D., Brøndum-Nielsen, K., Tümer, Z. (2013) Microduplication of 15q13.3 and Xq21.31 in a family with Tourette syndrome and comorbidities. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 162B, 825–831.
70. Taske, N. L., Williamson, M. P., Makoff, A., Bate, L., Curtis, D., Kerr, M., Kjeldsen, M. J., Pang, K. A., Sundqvist, A., Friis, M. L., Chadwick, D., Richens, A., Covanis, A., Santos, M., Arzimanoglou, A., Panayiotopoulos, C. P., Whitehouse, W. P., Rees, M., Gardiner, R. M. (2002) Evaluation of the positional candidate gene CHRNA7 at the juvenile myoclonic epilepsy locus (EJM2) on chromosome 15q13-14. Epilepsy Res. 49, 157–172.
71. Rozycka, A., Dorszewska, J., Steinborn, B., Kempisty, B., Lianeri, M., Wisniewska, K., Jagodzinski, P. P. (2013) A transcript coding for a partially duplicated form of a7 nicotinic acetylcholine receptor is absent from the CD4+ T-lymphocytes of patients with autosomal dominant nocturnal frontal lobe epilepsy (ADNFLE). Folia Neuropathol. 51, 65–75.
72. Rozycka, A., Dorszewska, J., Steinborn, B., Lianeri, M., Winczewska- Wiktor, A., Sniezawska, A., Wisniewska, K., Jagodzinski, P. P. (2013) Association study of the 2-bp deletion polymorphism in exon 6 of the CHRFAM7A gene with idiopathic generalized epilepsy. DNA Cell Biol. 32, 640–647.
73. Thierry-Mieg, D., Thierry-Mieg, J. (2006) AceView: a comprehensive cDNA-supported gene and transcripts annotation. Genome Biol. 7 (Suppl 1), S12.1–14.
74. Wang, Y., Xiao, C., Indersmitten, T., Freedman, R., Leonard, S., Lester, H. A. (2014) The duplicated alpha7 subunits assemble and form functional nicotinic receptors with the full-length alpha 7. J. Biol. Chem. 289, 26451–26463
75. Perl, O., Strous, R. D., Dranikov, A., Chen, R., Fuchs, S. (2006) Low levels of alpha7-nicotinic acetylcholine receptor mRNA on peripheral blood lymphocytes in schizophrenia and its association with illness severity. Neuropsychobiology 53, 88–93.
76. Severance, E. G., Dickerson, F. B., Stallings, C. R., Origoni, A. E., Sullens, A., Monson, E. T., Yolken, R. H. (2009) Differentiating nicotineversus schizophrenia-associated decreases of the alpha7 nicotinic acetylcholine receptor transcript, CHRFAM7A, in peripheral blood lymphocytes. J. Neural Transm. 116, 213–220.
77. Gault, J., Hopkins, J., Berger, R., Drebing, C., Logel, J., Walton, C., Short, M., Vianzon, R., Olincy, A., Ross, R. G., Adler, L. E., Freedman, R., Leonard, S. (2003) Comparison of polymorphisms in the alpha7 nicotinic receptor gene and its partial duplication in schizophrenic and control subjects. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 123B, 39–49.
78. Severance, E. G., Zhang, H., Cruz, Y., Pakhlevaniants, S., Hadley, S. H., Amin, J., Wecker, L., Reed, C., Cuevas, J. (2004) The alpha7 nicotinic acetylcholine receptor subunit exists in two isoforms that contribute to functional ligand-gated ion channels. Mol. Pharmacol. 66, 420–429.
79. Kaufman, R. L., Oger, J. (1989) Search for nicotinic acetylcholine receptors on human leukocytes: absence of alpha-bungarotoxin binding in studies of healthy individuals and myasthenia gravis patients. J. Neuroimmunol. 23, 83–87.
80. Richman, D. P., Arnason, B. G. (1979) Nicotinic acetylcholine receptor: evidence for a functionally distinct receptor on human lymphocytes. Proc. Natl. Acad. Sci. USA 76, 4632–4635.
81. Richman, D. P., Antel, J. P., Burns, J. B., Arnason, B. G. (1981) Nicotinic acetylcholine receptor on human lymphocytes. Ann. N. Y. Acad. Sci. 377, 427–435.
82. Atweh, S. F., Grayhack, J. J., Richman, D. P. (1984) A cholinergic receptor site on murine lymphocytes with novel binding characteristics. Life Sci. 35, 2459–2469.
83. Engel, E. K., Trotter, J. L., McFarlin, D. E., McIntosh, C. L. (1977) Thymic epithelial cell contains acetylcholine receptor. Lancet 1, 1310–1311.
84. Mizuno, Y., Dosch, H. M., Gelfand, E. W. (1982) Carbamycholine modulation of E-rosette formation: identification of nicotinic acetylcholine receptors on a subpopulation of human T lymphocytes. J. Clin. Immunol. 2, 303–308.
85. Davies, B. D., Hoss, W., Lin, J. P., Lionetti, F. (1982) Evidence for a noncholinergic nicotine receptor on human phagocytic leukocytes. Mol. Cell. Biochem. 44, 23–31.
86. Marks, M. J., Collins, A. C. (1982) Characterization of nicotine binding in mouse brain and comparison with the binding of alpha-bungarotoxin and quinuclidinyl benzilate. Mol. Pharmacol. 22, 554–564.
87. Whaley, K., Lappin, D., Barkas, T. (1981) C2 synthesis by human monocytes is modulated by a nicotinic cholinergic receptor. Nature 293, 580–583.
88. Benfante, R., Antonini, R. A., De Pizzol, M., Gotti, C., Clementi, F., Locati, M., Fornasari, D. (2011) Expression of the a7 nAChR subunit duplicate form (CHRFAM7A) is down-regulated in the monocytic cell line THP-1 on treatment with LPS. J. Neuroimmunol. 230, 74–84.
89. Van der Zanden, E. P., Hilbers, F. W., Verseijden, C., van den Wijngaard, R. M., Skynner, M., Lee, K., Ulloa, L., Boeckxstaens, G. E., de Jonge, W. J. (2012) Nicotinic acetylcholine receptor expression and susceptibility to cholinergic immunomodulation in human monocytes of smoking individuals. Neuroimmunomodulation 19, 255–265.
90. Yasui, D. H., Scoles, H. A., Horike, S., Meguro-Horike, M., Dunaway, K. W., Schroeder, D. I., Lasalle, J. M. (2011) 15q11.2-13.3 Chromatin analysis reveals epigenetic regulation of CHRNA7 with deficiencies in Rett and autism brain. Hum. Mol. Genet. 20, 4311–4323.
91. Araud, T., Graw, S., Berger, R., Lee, M., Neveu, E., Bertrand, D., Leonard, S. (2011) The chimeric gene CHRFAM7A, a partial duplication of the CHRNA7 gene, is a dominant negative regulator of a7*nAChR function. Biochem. Pharmacol. 82, 904–914.
92. De Lucas-Cerrillo, A. M., Maldifassi, M. C., Arnalich, F., Renart, J., Atienza, G., Serantes, R., Cruces, J., Sánchez-Pacheco, A., Andrés- Mateos, E., Montiel, C. (2011) Function of partially duplicated human a77 nicotinic receptor subunit CHRFAM7A gene: potential implications for the cholinergic anti-inflammatory response. J. Biol. Chem. 286, 594–606.
93. Hurst, R. S., Hajós, M., Raggenbass, M., Wall, T. M., Higdon, N. R., Lawson, J. A., Rutherford-Root, K. L., Berkenpas, M. B., Hoffmann, W. E., Piotrowski, D. W., Groppi, V. E., Allaman, G., Ogier, R., Bertrand, S., Bertrand, D., Arneric, S. P. (2005) A novel positive allosteric modulator of the alpha7 neuronal nicotinic acetylcholine receptor: in vitro and in vivo characterization. J. Neurosci. 25, 4396–4405.
94. Kaessmann, H. (2010) Origins, evolution, and phenotypic impact of new genes. Genome Res. 20, 1313–1326.
95. Li, C. Y., Zhang, Y., Wang, Z., Zhang, Y., Cao, C., Zhang, P. W., Lu, S. J., Li, X. M., Yu, Q., Zheng, X., Du, Q., Uhl, G. R., Liu, Q. R., Wei, L. (2010) A human-specific de novo protein-coding gene associated with human brain functions. PLOS Comput. Biol. 6, e1000734.
96. Long, M., Betrán, E., Thornton, K., Wang, W. (2003) The origin of new genes: glimpses from the young and old. Nat. Rev. Genet. 4, 865–875.
97. Ohno, S. (1970) Evolution by Gene Duplication. Springer-Verlag, Heidelberg, Germany.
98. Toll-Riera, M., Bosch, N., Bellora, N., Castelo, R., Armengol, L., Estivill, X., Albà, M. M. (2009) Origin of primate orphan genes: a comparative genomics approach. Mol. Biol. Evol. 26, 603–612.
99. Wu, D. D., Irwin, D. M., Zhang, Y. P. (2011) De novo origin of human protein-coding genes. PLoS Genet. 7, e1002379.
100. Stahl, P. D., Wainszelbaum, M. J. (2009) Human-specific genes may offer a unique window into human cell signaling. Sci. Signal. 2, pe59.
101. Nahon, J. L. (2003) Birth of ‘human-specific’ genes during primate evolution. Genetica 118, 193–208.
102. Huang, H., Winter, E. E., Wang, H., Weinstock, K. G., Xing, H., Goodstadt, L., Stenson, P. D., Cooper, D. N., Smith, D., Albà, M. M., Pointing, C. P., Fechtel, K. (2004) Evolutionary conservation and selection of human disease gene orthologs in the rat and mouse genomes. Genome Biol. 5, R47.
103. Tu, Z., Wang, L., Xu, M., Zhou, X., Chen, T., Sun, F. (2006) Further understanding human disease genes by comparing with housekeeping genes and other genes. BMC Genomics 7, 31.
104. Cooper, D. N., Kehrer-Sawatzki, H. (2011) Exploring the potential relevance of human-specific genes to complex disease. Hum. Genomics 5, 99–107.
105. National Institute of General Medical Sciences, National Institutes of Health. (2001) Glue Grant Inflammation and the Host Response to Injury. Massachusetts General Hospital, Boston, from https://www.gluegrant.org/.
106. Osuchowski, M. F., Remick, D. G., Lederer, J. A., Lang, C. H., Aasen, A. O., Aibiki, M., Azevedo, L. C., Bahrami, S., Boros, M., Cooney, R., Cuzzocrea, S., Jiang, Y., Junger, W. G., Hirasawa, H., Hotchkiss, R. S., Li, X. A., Radermacher, P., Redl, H., Salomao, R., Soebandrio, A., Thiemermann, C., Vincent, J. L., Ward, P., Yao, Y. M., Yu, H. P., Zingarelli, B., Chaudry, I. H. (2014) Abandon the mouse research ship? Not just yet! Shock 41, 463–475.
107. Seok, J., Warren, H. S., Cuenca, A. G., Mindrinos, M. N., Baker, H. V., Xu, W., Richards, D. R., McDonald-Smith, G. P., Gao, H., Hennessy, L., Finnerty, C. C., López, C. M., Honari, S., Moore, E. E., Minei, J. P., Cuschieri, J., Bankey, P. E., Johnson, J. L., Sperry, J., Nathens, A. B., Billiar, T. R., West, M. A., Jeschke, M. G., Klein, M. B., Gamelli, R. L., Gibran, N. S., Brownstein, B. H., Miller-Graziano, C., Calvano, S. E., Mason, P. H., Cobb, J. P., Rahme, L. G., Lowry, S. F., Maier, R. V., Moldawer, L. L., Herndon, D. N., Davis, R. W., Xiao, W., Tompkins, R. G.; Inflammation and Host Response to Injury, Large Scale Collaborative Research Program. (2013) Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc. Natl. Acad. Sci. USA 110, 3507–3512.
108. Takao, K., Miyakawa, T. (2014) Genomic responses in mouse models greatly mimic human inflammatory diseases. Proc. Natl. Acad. Sci. USA doi:10.1073/pnas.1401965111 [Epub ahead of print].
109. Xiao, W., Mindrinos, M. N., Seok, J., Cuschieri, J., Cuenca, A. G., Gao, H., Hayden, D. L., Hennessy, L., Moore, E. E., Minei, J. P., Bankey, P. E., Johnson, J. L., Sperry, J., Nathens, A. B., Billiar, T. R., West, M. A., Brownstein, B. H., Mason, P. H., Baker, H. V., Finnerty, C. C., Jeschke, M. G., López, M. C., Klein, M. B., Gamelli, R. L., Gibran, N. S., Arnoldo, B., Xu, W., Zhang, Y., Calvano, S. E., McDonald-Smith, G. P., Schoenfeld, D. A., Storey, J. D., Cobb, J. P., Warren, H. S., Moldawer, L. L., Herndon, D. N., Lowry, S. F., Maier, R. V., Davis, R. W., Tompkins, R. G.; Inflammation and Host Response to Injury Large-Scale Collaborative Research Program. (2011) A genomic storm in critically injured humans. J. Exp. Med. 208, 2581–2590.
110. Hedlund, M., Tangvoranuntakul, P., Takematsu, H., Long, J. M., Housley, G. D., Kozutsumi, Y., Suzuki, A., Wynshaw-Boris, A., Ryan, A. F., Gallo, R. L., Varki, N., Varki, A. (2007) N-Glycolylneuraminic acid deficiency in mice: implications for human biology and evolution. Mol. Cell. Biol. 27, 4340–4346.