ORIGINAL RESEARCH–SINONASAL DISORDERS
Murine complement deficiency ameliorates acute
cigarette smoke-induced nasal damage
Kara S. Davis, Sarah E. Casey, Jennifer K. Mulligan, PhD,
Ryan M. Mulligan, MS, Rodney J. Schlosser, MD, and Carl Atkinson, PhD,
Charleston, SC
Sponsorships or competing interests that may be relevant to con-
tent are disclosed at the end of this article.
ABSTRACT
OBJECTIVE: Exposure to cigarette smoke is a risk factor for
chronic rhinosinusitis. Current literature confirms complement
fragments are activated in human nasal mucosa. The mechanism(s)
responsible for this activation is unclear. We investigated the
effects of cigarette smoke on nasal mucosa in vitro and via a model
of cigarette smoke exposure by using animals deficient in comple-
ment components.
STUDY DESIGN: Prospective, controlled animal and in vitro
human cell line study.
SETTING: University laboratory.
SUBJECTS AND METHODS: Human respiratory epithelial
cells were exposed to five, 10, and 20 percent cigarette smoke
extract (CSE) in vitro in the presence or absence of human serum.
Complement activation was assessed by enzyme-linked immu-
nosorbent assay and immunofluorescent techniques. Complement-
deficient (C3
–/–
,n = 6; factor B
–/–
,n = 50) and sufficient mice
(wild type, n = 10) were exposed to the smoke of four cigarettes
per exposure for two exposures per day for three days. Mice were
sacrificed 12 hours after the last exposure, and the nasal cavity was
surgically removed. Histological characteristics were analyzed by
the use of a subjective scale and quantitative image analysis
scoring systems.
RESULTS: In vitro analysis of respiratory cell cultures demon-
strated that exposure of serum to CSE resulted in complement
activation. Furthermore, immunofluorescent staining for C3d
could only be demonstrated in CSE-exposed cultures. In vivo
analysis demonstrated that complement deficiency, either C3 or
factor B deficiency, resulted in a significant reduction in histolog-
ical evidence of damage as compared with wild-type control mice
(wild type vs C3
–/–
, P = 0.02; wild type vs factor B
–/–
, P = 0.07;
no significant difference between C3
–/–
vs factor B
–/–
).
CONCLUSION: These data demonstrate that cigarette smoke
activates the complement system. Furthermore, complement defi-
ciency protected against smoke-induced mucosal damage in this
small series.
© 2010 American Academy of Otolaryngology–Head and Neck
Surgery Foundation. All rights reserved.
E
ach year, chronic rhinosinusitis (CRS) is estimated to
affect 14 percent of the adult U.S. population.
1
Not
surprisingly, CRS is repeatedly found to have an adverse
impact on the daily activities, productivity, and cognitive
function of patients.
Despite these widespread negative consequences, the
treatment of CRS apart from surgical intervention remains
largely symptomatic and often does not induce remission of
underlying mucosal inflammation. Expertly defined as “in-
flammatory conditions involving the paranasal sinuses, as
well as the lining of the nasal passages that persist beyond
12 weeks,” a more complete understanding of the inflam-
mation characterizing CRS and its mechanism(s) is re-
garded as the gateway to developing more definitive treat-
ment options.
2
Furthermore, as new types of therapeutic
options are developed for other diseases, understanding the
pathogenesis of CRS is crucial to predict the therapeutic
outcomes of CRS patients to these novel treatments and to
research them appropriately.
3
Until recently, much of the study of CRS pathogenesis
focused on the adaptive immune system in isolation, includ-
ing the relative balance of T helper cell 1 versus T helper
cell 2 (Th
2
) cytokine milieu in response to ubiquitous en-
vironmental stimuli, such as bacteria and fungi. These lines
of evidence, however, do not explain why only some sub-
jects develop CRS and other related conditions to pathogens
to which nearly all humans are exposed. Environmental
stimuli presented to a person’s nasal mucosa are not unique
pathogens; it seems plausible that variations in individual
immunologic responses to otherwise-ubiquitous stimuli
may contribute to the development of CRS. An emerging
theory is the role of the innate immune system and, more
important, how it interacts with and modifies responses of
the adaptive immune system to induce deregulated immune
responses leading to chronic inflammation.
Innate immunity is the basic defense of the sinonasal
cavity, including anatomical and physiological features of
the epithelium, which functions to limit the penetration of
environmental stimuli and pathogens, thereby lessening the
Received October 17, 2009; revised February 4, 2010; accepted February 16, 2010.
Otolaryngology–Head and Neck Surgery (2010) 143, 152-158
0194-5998/$36.00 © 2010 American Academy of Otolaryngology–Head and Neck Surgery Foundation. All rights reserved.
doi:10.1016/j.otohns.2010.02.022