Protein & Peptide Letters
Monika A. Coronado
a,b
, Icaro P. Caruso
b
, Vinícius M. de Oliveira
b
, Vinícius G. Contessoto
b
,
Vitor B.P. Leite
b
, Liege A. Kawai
a,b
, Raghuvir K. Arni
a,b
and Raphael J. Eberle
a,b,
*
a
Multiuser Center for Biomolecular Innovation, Universidade Estadual Paulista (UNESP), São Jose do Rio Preto-SP,
15054-000, Brazil;
b
Department of Physics, Universidade Estadual Paulista (UNESP), São Jose do Rio Preto-SP,
15054-000, Brazil
A R T I C L E H I S T O R Y
Received: November 30, 2016
Revised: January 25, 2017
Accepted: January 25, 2017
DOI: 10.2174/0929866524666170207
153808
Abstract: The conformational stability of the Cold shock protein A (CspA) from C. pseudotubercu-
losis (Cp), a nucleic acid binding protein in function of pH and salt concentration was examined by
using differential scanning calorimetry and CD spectroscopy in combination with computational
analysis to identify the specify amino acids undergoing change. Our approach identified a sodium-
binding site in CpCspA and at pH 8.0 a significant reduction in the β-sheet content was observed
which resulted in a decrease of the protein thermal stability. The computational analyses identified
His30 and His65 as the amino acids with the largest charge shifts at different pHs. His30/His65 are
part of the extensive hydrogen bonding network and along with the ion-binding site are essential for
the conformational stability of CspA.
Keywords: Cold shock protein, C. pseudotuberculosis, ion binding, histidine, pH, secondary structure.
1. INTRODUCTION
Bacteria respond to changes in environmental parameters
such as nutrient levels, oxygen availability, osmotic stress
and temperature by triggering the activation of a specific set
of genes that up-regulate the production of cold shock pro-
teins (Csps) and consequently, by restricting the production
of non-cold-shock proteins [1-3].
The initial phase of the cold shock response, the acclima-
tion phase, is characterized by high levels of expression of
Csp which stimulates the synthesis of other cold-stress re-
lated proteins [4, 5]. At the end of the acclimation phase the
synthesis of the cold shock proteins is diminished and the
levels of non-cold shock protein synthesis are reestablished
[6]. The primary function of Csps involves the enhancement
of DNA transcription to support the expression of other cold
shock induced genes [5, 7, 8]. This is achieved by the high
affinity and specificity of Csps in binding to short single-
stranded DNAs [9-12]. The observed non-specific binding of
Csps to ssRNA suggests that they could also function as
RNA chaperones [13] by preventing the formation of
cold-induced mRNA secondary structures [14]. Both mecha-
nisms help to preserve cell viability during the cold shock
process and also in restoring normal cell functions.
*Address correspondence to this author at the Multiuser Center for Bio-
molecular Innovation, Universidade Estadual Paulista (UNESP), Rua
Cristóvão Colombo 2265, São Jose do Rio Preto-SP, 15054-000, Brazil;
Tel/Fax: +55-17-32212707, +55-17-32212247;
E-mail: eberleraphael@gmail.co
Csps are encountered in a wide range of bacterial species,
such as psychrophilics, mesophilics, thermophilics and hy-
perthermophilics and share highly conserved sequences and
structural motifs. The three-dimensional structures of a num-
ber of Csps have been determined, including the E. coli
CspA, B. subtilis CspB, and B. caldolyticus CspB, and they
possess a typical β-barrel fold, consisting of a three stranded
N-terminal sheet (β1-β2-β3) and a two stranded C-terminal
sheet (β4-β5). Csps contain two nucleic acid binding motifs
(RNP1 and RNP2) consisting mainly of aromatic and basic
amino acid residues that participate in the binding to single-
stranded nucleic acids [15-18].
Despite the high degree of conservation of Csps se-
quences and principal structural motifs, the thermal stability
of these proteins varies significantly; the E. coli CspA un-
folds at 60 °C [16, 19], whereas the B. subtilis CspB unfolds
at 52 °C [10]. The melting temperature (T
m
) of the thermo-
philic B. caldolyticus Csp is 77 °C [17], twenty-five degrees
higher than the T
m
of B. subtilis CspB, and the reversible
unfolding process is a monomolecular (N) ↔ unfolded (U)
two state reaction [20]. Theoretical and experimental inves-
tigations on the thermal stability of Csps have examined the
role of point mutations [21], variations of salt concentration
[17, 22] and pH [23, 24].
Mycobacterium, Nocardia, and Rhodococcus), a cluster
of gram-positive bacteria species [25]. C. pseudotuberculosis
is the causative agent of caseous lymphadenitis (CLA), a
disease encountered in sheep, goats, and equids (ulcerative
lymphangitis) and cattle (cutaneous excoriated granulomas)
which results in drastically reduced yields of wool and milk,
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358
Protein & Peptide Letters, 2017, 24, 358-367
RESEARCH ARTICLE
Cold Shock Protein A from Corynebacterium pseudotuberculosis: Role of
Electrostatic Forces in the Stability of the Secondary Structure