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This Article Appeared in a Journal Published by Elsevier. the Attached This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Neuropeptides 45 (2011) 49–53 Contents lists available at ScienceDirect Neuropeptides journal homepage: www.elsevier.com/locate/npep Altered host response to murine gammaherpesvirus 68 infection in mice lacking the tachykinin 1 gene and the receptor for substance P John P. Quinn c, Anja Kipar b, David J. Hughes a, Elaine Bennett a, Helen Cox a, ⇑ Lynn McLaughlin c, Andreas Zimmer d, Stephen P. Hunt e, James P. Stewart a, a School of Infection and Host Defence, University of Liverpool, Liverpool, UK b Department of Veterinary Pathology, University of Liverpool, Liverpool, UK c Institute of Translational Medicine, University of Liverpool, Liverpool, UK d Institute of Molecular Psychiatry, University of Bonn, Germany e Research Department of Cell and Developmental Biology, University College London, UK article info abstract Article history: The tachykinins are implicated in neurogenic inflammation and the neuropeptide substance P in particular Received 8 June 2010 has been shown to be a proinflammatory mediator. A role for the tachykinins in host response to viral infec- Accepted 16 October 2010 tion has been previously demonstrated using either TAC1- or NK1 receptor-deficient transgenic mice. How- Available online 23 November 2010 ever, due to redundancy in the peptide–receptor complexes we wished determine whether a deficiency in TAC1 and NK1R in combination exhibited an enhanced phenotype. TAC1 and NK1R-deficient mice were Keywords: therefore crossed to generate transgenic mice in both (NK1À/À  TAC1À/À). As expected, after infection with Virus the respiratory pathogen murine gammaherpesvirus (MHV-68), TAC1 and NK1R-deficient mice were more Tachykinin susceptible to infection than wild-type C57BL/6 controls. However, unexpectedly, NK1À/À TAC1À/À mice Substance P  NK1 were more resistant to infection arguing for a lack of feedback inhibition through alternative receptors in Transgenic mice these mice. Histopathological examination did not show any great differences in the inflammatory responses between groups of infected animals, except for the presence of focal perivascular B cell accumu- lations in lungs of all the knockout mice. These were most pronounced in the NK1À/À  TAC1À/À mice. These results confirm an important role for TAC1 and NK1R in the control of viral infection but reinforce the com- plex nature of the peptide–receptor interactions. Ó 2010 Elsevier Ltd. All rights reserved. 1. Introduction system but is also involved in direct interaction between immune cells in a paracrine and/or autocrine fashion independent of sen- The tachykinin family of neurotransmitters are not only in- sory nerves (Ho et al., 1997; Lai et al., 1998). The tachykinins can volved in central and peripheral nervous system function but also modulate the immune response and SP has been shown to regulate have a role in inflammation (termed neurogenic inflammation) and production of a number of cytokines including IL-1, IL-6, IL-8 and adaptive immunity (Goetzl and Sreedharan, 1992; Maggi, 1997). TNFa to mediate inflammatory and cell proliferative responses The most characterized member of the family is substance P (SP). (Lotz et al., 1988; Palma and Manzini, 1998). This is encoded by the preprotachykinin A (PPT-A)orTAC1 locus. We have previously addressed the actions of the TAC1 gene Alternative splicing of TAC1 RNA and processing of the propeptide expression and function in virus infection in the lung and in partic- yields, in addition to SP, neurokinin A (NKA) and neuropeptides K ular early function of neuropeptides released from non-neuronal and c. Although local nerves have been believed to be the major cells in the lung. The tachykinins have been extensively implicated source of tachykinins in the peripheral tissues, TAC1 has been in the initiation and progression of lung disease processes such as shown to be induced and expressed in other cell types such as bronchitis and asthma (D’Agostino et al., 2002; Joos et al., 2000; monocytes, macrophages, pancreatic islet cells and various tumour Kamijo et al., 2001; Noveral and Grunstein, 1995), although it cell types (Germonpre et al., 1999; Ho et al., 1997; Lambrecht et al., was presumed that it was the release from sensory ganglia that 1999; McGregor et al., 1995; Singh et al., 2000). This has led to the was the major effector. A number of studies have shown that hypothesis that SP not only acts as a mediator of the neuroimmune viruses (e.g. respiratory syncytial virus and murine gammaherpes- virus, MHV-68) can induce SP and neurogenic inflammation, particularly in lungs in the context of a respiratory challenge ⇑ Corresponding author. Address: School of Infection and Host Defence, The University of Liverpool, Duncan Building, Daulby Street, Liverpool L69 3GA, UK. Tel.: (Payne et al., 2001; Piedimonte et al., 1999; Tripp et al., 2000). +44 151 706 4385; fax: +44 151 706 5805. Consistent with this NK1 is upregulated in lymphocytes (especially E-mail addresses: [email protected], [email protected] (J.P. Stewart). T cells) in the lung in response to viral infection in the lung (Tripp 0143-4179/$ - see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.npep.2010.10.004 Author's personal copy 50 J.P. Quinn et al. / Neuropeptides 45 (2011) 49–53 et al., 2002) and antibody to SP decreases inflammatory responses the offspring were null mutants at both the NK1 and Tac1 loci. These to pulmonary viral infection (Haynes et al., 2002). This indicates a mice were breed and the double knockout line was maintained with primary role for SP in the lung in the response to respiratory viral sister  brother mating. This breeding strategy was chosen to ad- infection. More recently we have demonstrated in a transgenic here to the 3Rs (reduction, replacement, refinement) with regards model in which the TAC1 gene is co-expressed with the LacZ mar- to reduction of mice with unwanted genotype and to maximise dou- ker gene (MacKenzie et al., 2000; MacKenzie and Quinn, 2002) that ble knockout survival chances (refinement). Males and females non-neuronal TAC1 expression early after infection may have were separated at weaning (19–21 days after birth) and housed in important clinical implications for the progression or management conventional cages. They were grouped up to six animals per cage of lung disease or infection aside from the well characterized later for maintenance under standard conditions (12 h light/dark cycle, involvement of the tachykinins during the inflammatory response 22 ± 1 °C ambient temperature, 60% relative humidity, food and (Stewart et al., 2008). The action of MHV-68 is similar to that of water provided ad libitum). RSV in the lung as regards tachykinin expression and function in R which SP is increased (Dakhama et al., 2005) and altered NK1 2.3. Infection of animals expression is observed (Piedimonte, 2003). This alteration of tach- ykinin function and expression is observed in other challenges in Animals 5–7 weeks of age were anesthetized with halothane and the lung (Hegde et al., 2007; Ng et al., 2008; Puneet et al., 2006; inoculated with 4  105 plaque forming units (PFU) in 40 ll of ster- Zhang et al., 2007). We therefore view the tachykinin pathway as ile phosphate buffered saline (PBS). At various times between day 3 a key major modulator of the immune response to lung challenge. and 40 p.i., animals were euthanized and tissues were harvested. Experiments are usually done with either knock outs of the neu- ropeptide gene (TAC1) or the high affinity receptor (NK1R). These 2.4. Real-time quantitative PCR analysis knockouts have been generated on a variety of strains and strain differences have been demonstrated to have a major affect on bio- To determine the viral DNA (vDNA) load, DNA was extracted logical importance. Further, in addition to the classical peptides SP from splenic and pulmonary tissue using DNeasy kits (Qiagen) and NKA, the recently discovered peptides such as hemokinin 1 and quantified by UV spectrophotometry. Quantification of vDNA and the endokinins have been found in non-neuronal cells/tissues copy number was performed using an Opticon Monitor 2 real-time such as pulmonary and cardiovascular tissue, articular cartilage PCR machine (MJ Research) using primers specific for the MHV-68 and cells of the immune system (Zhang et al., 2000; Zhang and gp150 gene as described previously (Hughes et al., 2010). Copy Paige, 2003) and they signal through affinity SP receptors, NK-1R numbers were normalized relative to the murine ribosomal protein (Morteau et al., 2001) adding a further layer of complexity to the L8 (rpl8) gene mean viral genome copy numbers were determined tachykinin function in host defense. Given the redundancy and from four individual animals. Statistical analysis was performed complexity in tachykinin peptides and receptors, we wished to using student’s T-test with a confidence limit of 95%. generate a more stringent knockout that defined tachykinin func- tion better. We surmised that a mouse lacking tachykinin peptides and high affinity receptor would address the problems of redun- 2.5. Histology, immunohistology and RNA-in situ hybridization dancy.
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